diff --git a/Emby.Server.Implementations/HttpServer/WebSocketConnection.cs b/Emby.Server.Implementations/HttpServer/WebSocketConnection.cs
index 373b0994a6..6dc6d9d289 100644
--- a/Emby.Server.Implementations/HttpServer/WebSocketConnection.cs
+++ b/Emby.Server.Implementations/HttpServer/WebSocketConnection.cs
@@ -1,5 +1,7 @@
 using System;
 using System.Buffers;
+using System.Collections.Generic;
+using System.Globalization;
 using System.IO.Pipelines;
 using System.Net;
 using System.Net.WebSockets;
@@ -7,6 +9,7 @@ using System.Text;
 using System.Text.Json;
 using System.Threading;
 using System.Threading.Tasks;
+using Emby.Server.Implementations.Localization;
 using Jellyfin.Extensions.Json;
 using MediaBrowser.Controller.Net;
 using MediaBrowser.Controller.Net.WebSocketMessages;
@@ -69,6 +72,17 @@ namespace Emby.Server.Implementations.HttpServer
         /// <inheritdoc />
         public IPAddress? RemoteEndPoint { get; }
 
+        /// <summary>
+        /// Gets or initializes the culture fallback chain captured from the
+        /// <c>Accept-Language</c> header of the upgrade request.
+        /// </summary>
+        public IReadOnlyList<string>? RequestCultureFallback { get; init; }
+
+        /// <summary>
+        /// Gets or initializes the UI culture name captured from the upgrade request.
+        /// </summary>
+        public string? RequestUICulture { get; init; }
+
         /// <inheritdoc />
         public Func<WebSocketMessageInfo, Task>? OnReceive { get; set; }
 
@@ -81,6 +95,28 @@ namespace Emby.Server.Implementations.HttpServer
         /// <inheritdoc />
         public WebSocketState State => _socket.State;
 
+        /// <inheritdoc />
+        public void ApplyRequestCulture()
+        {
+            if (RequestCultureFallback is not null)
+            {
+                LocalizationManager.RequestCultureFallback = RequestCultureFallback;
+            }
+
+            if (!string.IsNullOrEmpty(RequestUICulture))
+            {
+                try
+                {
+                    CultureInfo.CurrentUICulture = CultureInfo.GetCultureInfo(RequestUICulture);
+                }
+                catch (CultureNotFoundException)
+                {
+                    // Jellyfin culture codes (e.g. "es_419") aren't always valid .NET cultures —
+                    // skip setting CurrentUICulture; RequestCultureFallback above carries the chain.
+                }
+            }
+        }
+
         /// <inheritdoc />
         public async Task SendAsync(OutboundWebSocketMessage message, CancellationToken cancellationToken)
         {
diff --git a/Emby.Server.Implementations/HttpServer/WebSocketManager.cs b/Emby.Server.Implementations/HttpServer/WebSocketManager.cs
index cb5b3993b8..3b5f6d1d09 100644
--- a/Emby.Server.Implementations/HttpServer/WebSocketManager.cs
+++ b/Emby.Server.Implementations/HttpServer/WebSocketManager.cs
@@ -4,9 +4,11 @@
 
 using System;
 using System.Collections.Generic;
+using System.Globalization;
 using System.Linq;
 using System.Net.WebSockets;
 using System.Threading.Tasks;
+using Emby.Server.Implementations.Localization;
 using MediaBrowser.Common.Extensions;
 using MediaBrowser.Controller.Net;
 using Microsoft.AspNetCore.Http;
@@ -48,13 +50,22 @@ namespace Emby.Server.Implementations.HttpServer
 
                 WebSocket webSocket = await context.WebSockets.AcceptWebSocketAsync().ConfigureAwait(false);
 
+                // Capture the culture context set by AcceptLanguageMiddleware so it can be
+                // restored both when processing incoming messages and when periodic
+                // listeners produce server-initiated payloads on background tasks.
                 var connection = new WebSocketConnection(
                     _loggerFactory.CreateLogger<WebSocketConnection>(),
                     webSocket,
                     authorizationInfo,
                     context.GetNormalizedRemoteIP())
                 {
-                    OnReceive = ProcessWebSocketMessageReceived
+                    RequestCultureFallback = LocalizationManager.RequestCultureFallback,
+                    RequestUICulture = CultureInfo.CurrentUICulture.Name
+                };
+                connection.OnReceive = result =>
+                {
+                    connection.ApplyRequestCulture();
+                    return ProcessWebSocketMessageReceived(result);
                 };
                 await using (connection.ConfigureAwait(false))
                 {
diff --git a/Emby.Server.Implementations/Localization/Core/en-US.json b/Emby.Server.Implementations/Localization/Core/en-US.json
index 9b5049c8c7..ff674bd0d0 100644
--- a/Emby.Server.Implementations/Localization/Core/en-US.json
+++ b/Emby.Server.Implementations/Localization/Core/en-US.json
@@ -1,45 +1,29 @@
 {
-    "Albums": "Albums",
     "AppDeviceValues": "App: {0}, Device: {1}",
-    "Application": "Application",
     "Artists": "Artists",
     "AuthenticationSucceededWithUserName": "{0} successfully authenticated",
     "Books": "Books",
-    "CameraImageUploadedFrom": "A new camera image has been uploaded from {0}",
-    "Channels": "Channels",
     "ChapterNameValue": "Chapter {0}",
     "Collections": "Collections",
     "Default": "Default",
-    "DeviceOfflineWithName": "{0} has disconnected",
-    "DeviceOnlineWithName": "{0} is connected",
     "External": "External",
     "FailedLoginAttemptWithUserName": "Failed login attempt from {0}",
     "Favorites": "Favorites",
     "Folders": "Folders",
     "Forced": "Forced",
     "Genres": "Genres",
-    "HeaderAlbumArtists": "Album artists",
     "HeaderContinueWatching": "Continue Watching",
-    "HeaderFavoriteAlbums": "Favorite Albums",
-    "HeaderFavoriteArtists": "Favorite Artists",
     "HeaderFavoriteEpisodes": "Favorite Episodes",
     "HeaderFavoriteShows": "Favorite Shows",
-    "HeaderFavoriteSongs": "Favorite Songs",
     "HeaderLiveTV": "Live TV",
     "HeaderNextUp": "Next Up",
-    "HeaderRecordingGroups": "Recording Groups",
     "HearingImpaired": "Hearing Impaired",
     "HomeVideos": "Home Videos",
     "Inherit": "Inherit",
-    "ItemAddedWithName": "{0} was added to the library",
-    "ItemRemovedWithName": "{0} was removed from the library",
     "LabelIpAddressValue": "IP address: {0}",
     "LabelRunningTimeValue": "Running time: {0}",
     "Latest": "Latest",
-    "MessageApplicationUpdated": "Jellyfin Server has been updated",
-    "MessageApplicationUpdatedTo": "Jellyfin Server has been updated to {0}",
-    "MessageNamedServerConfigurationUpdatedWithValue": "Server configuration section {0} has been updated",
-    "MessageServerConfigurationUpdated": "Server configuration has been updated",
+    "LyricDownloadFailureFromForItem": "Lyrics failed to download from {0} for {1}",
     "MixedContent": "Mixed content",
     "Movies": "Movies",
     "Music": "Music",
@@ -66,24 +50,15 @@
     "NotificationOptionVideoPlaybackStopped": "Video playback stopped",
     "Original": "Original",
     "Photos": "Photos",
-    "Playlists": "Playlists",
-    "Plugin": "Plugin",
     "PluginInstalledWithName": "{0} was installed",
     "PluginUninstalledWithName": "{0} was uninstalled",
     "PluginUpdatedWithName": "{0} was updated",
-    "ProviderValue": "Provider: {0}",
     "ScheduledTaskFailedWithName": "{0} failed",
-    "ScheduledTaskStartedWithName": "{0} started",
-    "ServerNameNeedsToBeRestarted": "{0} needs to be restarted",
     "Shows": "Shows",
-    "Songs": "Songs",
     "StartupEmbyServerIsLoading": "Jellyfin Server is loading. Please try again shortly.",
     "SubtitleDownloadFailureFromForItem": "Subtitles failed to download from {0} for {1}",
-    "Sync": "Sync",
-    "System": "System",
     "TvShows": "TV Shows",
     "Undefined": "Undefined",
-    "User": "User",
     "UserCreatedWithName": "User {0} has been created",
     "UserDeletedWithName": "User {0} has been deleted",
     "UserDownloadingItemWithValues": "{0} is downloading {1}",
@@ -91,11 +66,8 @@
     "UserOfflineFromDevice": "{0} has disconnected from {1}",
     "UserOnlineFromDevice": "{0} is online from {1}",
     "UserPasswordChangedWithName": "Password has been changed for user {0}",
-    "UserPolicyUpdatedWithName": "User policy has been updated for {0}",
     "UserStartedPlayingItemWithValues": "{0} is playing {1} on {2}",
     "UserStoppedPlayingItemWithValues": "{0} has finished playing {1} on {2}",
-    "ValueHasBeenAddedToLibrary": "{0} has been added to your media library",
-    "ValueSpecialEpisodeName": "Special - {0}",
     "VersionNumber": "Version {0}",
     "TasksMaintenanceCategory": "Maintenance",
     "TasksLibraryCategory": "Library",
@@ -121,8 +93,8 @@
     "TaskUpdatePluginsDescription": "Downloads and installs updates for plugins that are configured to update automatically.",
     "TaskCleanTranscode": "Clean Transcode Directory",
     "TaskCleanTranscodeDescription": "Deletes transcode files more than one day old.",
-    "TaskRefreshChannels": "Refresh Channels",
-    "TaskRefreshChannelsDescription": "Refreshes internet channel information.",
+    "TasksRefreshChannels": "Refresh Channels",
+    "TasksRefreshChannelsDescription": "Refreshes internet channel information.",
     "TaskDownloadMissingLyrics": "Download missing lyrics",
     "TaskDownloadMissingLyricsDescription": "Downloads lyrics for songs",
     "TaskDownloadMissingSubtitles": "Download missing subtitles",
diff --git a/Emby.Server.Implementations/Localization/LocalizationManager.cs b/Emby.Server.Implementations/Localization/LocalizationManager.cs
index d8797e612b..2a7a3388aa 100644
--- a/Emby.Server.Implementations/Localization/LocalizationManager.cs
+++ b/Emby.Server.Implementations/Localization/LocalizationManager.cs
@@ -3,10 +3,12 @@ using System.Collections.Concurrent;
 using System.Collections.Frozen;
 using System.Collections.Generic;
 using System.Diagnostics.CodeAnalysis;
+using System.Globalization;
 using System.IO;
 using System.Linq;
 using System.Reflection;
 using System.Text.Json;
+using System.Threading;
 using System.Threading.Tasks;
 using Jellyfin.Extensions;
 using Jellyfin.Extensions.Json;
@@ -26,21 +28,36 @@ namespace Emby.Server.Implementations.Localization
         private const string RatingsPath = "Emby.Server.Implementations.Localization.Ratings.";
         private const string CulturesPath = "Emby.Server.Implementations.Localization.iso6392.txt";
         private const string CountriesPath = "Emby.Server.Implementations.Localization.countries.json";
+        private const string CoreResourcePrefix = "Emby.Server.Implementations.Localization.Core.";
         private static readonly Assembly _assembly = typeof(LocalizationManager).Assembly;
         private static readonly string[] _unratedValues = ["n/a", "unrated", "not rated", "nr"];
 
+        /// <summary>
+        /// Gets the mapping from BCP-47 hyphenated culture codes to Jellyfin's underscore-based codes.
+        /// </summary>
+        public static readonly FrozenDictionary<string, string> Bcp47ToJellyfinMap = new Dictionary<string, string>(StringComparer.OrdinalIgnoreCase)
+        {
+            ["es-419"] = "es_419",
+            ["es-DO"] = "es_DO",
+            ["ur-PK"] = "ur_PK"
+        }.ToFrozenDictionary(StringComparer.OrdinalIgnoreCase);
+
         private readonly IServerConfigurationManager _configurationManager;
         private readonly ILogger<LocalizationManager> _logger;
 
         private readonly Dictionary<string, Dictionary<string, ParentalRatingScore?>> _allParentalRatings = new(StringComparer.OrdinalIgnoreCase);
 
-        private readonly ConcurrentDictionary<string, Dictionary<string, string>> _dictionaries = new(StringComparer.OrdinalIgnoreCase);
+        private static readonly AsyncLocal<IReadOnlyList<string>?> _requestCultureFallback = new();
+
+        private readonly ConcurrentDictionary<string, Dictionary<string, string>> _cultureOnlyDictionaries = new(StringComparer.OrdinalIgnoreCase);
 
         private readonly JsonSerializerOptions _jsonOptions = JsonDefaults.Options;
 
         private readonly ConcurrentDictionary<string, CultureDto?> _cultureCache = new(StringComparer.OrdinalIgnoreCase);
         private List<CultureDto> _cultures = [];
 
+        private static readonly IReadOnlyList<LocalizationOption> _localizationOptions = BuildLocalizationOptions();
+
         private FrozenDictionary<string, string> _iso6392BtoT = null!;
 
         /// <summary>
@@ -54,6 +71,41 @@ namespace Emby.Server.Implementations.Localization
         {
             _configurationManager = configurationManager;
             _logger = logger;
+
+            _configurationManager.ConfigurationUpdated += OnConfigurationUpdated;
+        }
+
+        /// <summary>
+        /// Gets or sets the per-request culture fallback chain resolved from Accept-Language.
+        /// Each entry is a Jellyfin culture code (e.g. "de", "nl", "en-US") in priority order.
+        /// </summary>
+        public static IReadOnlyList<string>? RequestCultureFallback
+        {
+            get => _requestCultureFallback.Value;
+            set => _requestCultureFallback.Value = value;
+        }
+
+        /// <summary>
+        /// Checks whether a translation resource file exists for the given culture code.
+        /// </summary>
+        /// <param name="culture">The culture code to check (e.g. "de", "pt-BR", "es_419").</param>
+        /// <returns><c>true</c> if an embedded translation resource exists for the culture.</returns>
+        public static bool HasTranslation(string culture)
+        {
+            var resourceName = CoreResourcePrefix + GetResourceFilename(culture);
+            return _assembly.GetManifestResourceInfo(resourceName) is not null;
+        }
+
+        private static void OnConfigurationUpdated(object? sender, EventArgs e)
+        {
+            if (sender is IServerConfigurationManager configManager)
+            {
+                var uiCulture = configManager.Configuration.UICulture;
+                if (!string.IsNullOrEmpty(uiCulture))
+                {
+                    CultureInfo.DefaultThreadCurrentUICulture = new CultureInfo(uiCulture);
+                }
+            }
         }
 
         /// <summary>
@@ -419,6 +471,27 @@ namespace Emby.Server.Implementations.Localization
 
         /// <inheritdoc />
         public string GetLocalizedString(string phrase)
+        {
+            var fallback = _requestCultureFallback.Value;
+            if (fallback is not null)
+            {
+                foreach (var culture in fallback)
+                {
+                    var dict = GetLocalizationDictionary(culture);
+                    if (dict.TryGetValue(phrase, out var value))
+                    {
+                        return value;
+                    }
+                }
+
+                return phrase;
+            }
+
+            return GetLocalizedString(phrase, CultureInfo.CurrentUICulture.Name);
+        }
+
+        /// <inheritdoc />
+        public string GetServerLocalizedString(string phrase)
         {
             return GetLocalizedString(phrase, _configurationManager.Configuration.UICulture);
         }
@@ -436,6 +509,12 @@ namespace Emby.Server.Implementations.Localization
                 culture = DefaultCulture;
             }
 
+            // Normalize BCP-47 hyphenated codes to Jellyfin's underscore-based codes
+            if (Bcp47ToJellyfinMap.TryGetValue(culture, out var mapped))
+            {
+                culture = mapped;
+            }
+
             var dictionary = GetLocalizationDictionary(culture);
 
             if (dictionary.TryGetValue(phrase, out var value))
@@ -443,6 +522,15 @@ namespace Emby.Server.Implementations.Localization
                 return value;
             }
 
+            if (!string.Equals(culture, DefaultCulture, StringComparison.OrdinalIgnoreCase))
+            {
+                var fallback = GetLocalizationDictionary(DefaultCulture);
+                if (fallback.TryGetValue(phrase, out var fallbackValue))
+                {
+                    return fallbackValue;
+                }
+            }
+
             return phrase;
         }
 
@@ -450,28 +538,19 @@ namespace Emby.Server.Implementations.Localization
         {
             ArgumentException.ThrowIfNullOrEmpty(culture);
 
-            const string Prefix = "Core";
-
-            return _dictionaries.GetOrAdd(
+            return _cultureOnlyDictionaries.GetOrAdd(
                 culture,
-                static (key, localizationManager) => localizationManager.GetDictionary(Prefix, key, DefaultCulture + ".json").GetAwaiter().GetResult(),
+                static (key, localizationManager) =>
+                {
+                    var dictionary = new Dictionary<string, string>(StringComparer.OrdinalIgnoreCase);
+                    var namespaceName = localizationManager.GetType().Namespace + ".Core";
+                    localizationManager.CopyInto(dictionary, namespaceName + "." + GetResourceFilename(key)).GetAwaiter().GetResult();
+
+                    return dictionary;
+                },
                 this);
         }
 
-        private async Task<Dictionary<string, string>> GetDictionary(string prefix, string culture, string baseFilename)
-        {
-            ArgumentException.ThrowIfNullOrEmpty(culture);
-
-            var dictionary = new Dictionary<string, string>(StringComparer.OrdinalIgnoreCase);
-
-            var namespaceName = GetType().Namespace + "." + prefix;
-
-            await CopyInto(dictionary, namespaceName + "." + baseFilename).ConfigureAwait(false);
-            await CopyInto(dictionary, namespaceName + "." + GetResourceFilename(culture)).ConfigureAwait(false);
-
-            return dictionary;
-        }
-
         private async Task CopyInto(IDictionary<string, string> dictionary, string resourcePath)
         {
             using var stream = _assembly.GetManifestResourceStream(resourcePath);
@@ -508,77 +587,68 @@ namespace Emby.Server.Implementations.Localization
         /// <inheritdoc />
         public IEnumerable<LocalizationOption> GetLocalizationOptions()
         {
-            yield return new LocalizationOption("Afrikaans", "af");
-            yield return new LocalizationOption("العربية", "ar");
-            yield return new LocalizationOption("Беларуская", "be");
-            yield return new LocalizationOption("Български", "bg-BG");
-            yield return new LocalizationOption("বাংলা (বাংলাদেশ)", "bn");
-            yield return new LocalizationOption("Català", "ca");
-            yield return new LocalizationOption("Čeština", "cs");
-            yield return new LocalizationOption("Cymraeg", "cy");
-            yield return new LocalizationOption("Dansk", "da");
-            yield return new LocalizationOption("Deutsch", "de");
-            yield return new LocalizationOption("English (United Kingdom)", "en-GB");
-            yield return new LocalizationOption("English", "en-US");
-            yield return new LocalizationOption("Ελληνικά", "el");
-            yield return new LocalizationOption("Esperanto", "eo");
-            yield return new LocalizationOption("Español", "es");
-            yield return new LocalizationOption("Español americano", "es_419");
-            yield return new LocalizationOption("Español (Argentina)", "es-AR");
-            yield return new LocalizationOption("Español (Dominicana)", "es_DO");
-            yield return new LocalizationOption("Español (México)", "es-MX");
-            yield return new LocalizationOption("Eesti", "et");
-            yield return new LocalizationOption("Basque", "eu");
-            yield return new LocalizationOption("فارسی", "fa");
-            yield return new LocalizationOption("Suomi", "fi");
-            yield return new LocalizationOption("Filipino", "fil");
-            yield return new LocalizationOption("Français", "fr");
-            yield return new LocalizationOption("Français (Canada)", "fr-CA");
-            yield return new LocalizationOption("Galego", "gl");
-            yield return new LocalizationOption("Schwiizerdütsch", "gsw");
-            yield return new LocalizationOption("עִבְרִית", "he");
-            yield return new LocalizationOption("हिन्दी", "hi");
-            yield return new LocalizationOption("Hrvatski", "hr");
-            yield return new LocalizationOption("Magyar", "hu");
-            yield return new LocalizationOption("Bahasa Indonesia", "id");
-            yield return new LocalizationOption("Íslenska", "is");
-            yield return new LocalizationOption("Italiano", "it");
-            yield return new LocalizationOption("日本語", "ja");
-            yield return new LocalizationOption("Qazaqşa", "kk");
-            yield return new LocalizationOption("한국어", "ko");
-            yield return new LocalizationOption("Lietuvių", "lt");
-            yield return new LocalizationOption("Latviešu", "lv");
-            yield return new LocalizationOption("Македонски", "mk");
-            yield return new LocalizationOption("മലയാളം", "ml");
-            yield return new LocalizationOption("मराठी", "mr");
-            yield return new LocalizationOption("Bahasa Melayu", "ms");
-            yield return new LocalizationOption("Norsk bokmål", "nb");
-            yield return new LocalizationOption("नेपाली", "ne");
-            yield return new LocalizationOption("Nederlands", "nl");
-            yield return new LocalizationOption("Norsk nynorsk", "nn");
-            yield return new LocalizationOption("ਪੰਜਾਬੀ", "pa");
-            yield return new LocalizationOption("Polski", "pl");
-            yield return new LocalizationOption("Pirate", "pr");
-            yield return new LocalizationOption("Português", "pt");
-            yield return new LocalizationOption("Português (Brasil)", "pt-BR");
-            yield return new LocalizationOption("Português (Portugal)", "pt-PT");
-            yield return new LocalizationOption("Românește", "ro");
-            yield return new LocalizationOption("Русский", "ru");
-            yield return new LocalizationOption("Slovenčina", "sk");
-            yield return new LocalizationOption("Slovenščina", "sl-SI");
-            yield return new LocalizationOption("Shqip", "sq");
-            yield return new LocalizationOption("Српски", "sr");
-            yield return new LocalizationOption("Svenska", "sv");
-            yield return new LocalizationOption("தமிழ்", "ta");
-            yield return new LocalizationOption("తెలుగు", "te");
-            yield return new LocalizationOption("ภาษาไทย", "th");
-            yield return new LocalizationOption("Türkçe", "tr");
-            yield return new LocalizationOption("Українська", "uk");
-            yield return new LocalizationOption("اُردُو", "ur_PK");
-            yield return new LocalizationOption("Tiếng Việt", "vi");
-            yield return new LocalizationOption("汉语 (简体字)", "zh-CN");
-            yield return new LocalizationOption("漢語 (繁體字)", "zh-TW");
-            yield return new LocalizationOption("廣東話 (香港)", "zh-HK");
+            return _localizationOptions;
+        }
+
+        private static IReadOnlyList<LocalizationOption> BuildLocalizationOptions()
+        {
+            var options = new List<LocalizationOption>();
+            var prefix = CoreResourcePrefix;
+
+            foreach (var resource in _assembly.GetManifestResourceNames())
+            {
+                if (!resource.StartsWith(prefix, StringComparison.Ordinal)
+                    || !resource.EndsWith(".json", StringComparison.Ordinal))
+                {
+                    continue;
+                }
+
+                // Extract culture code from resource name: "...Core.de.json" -> "de", "...Core.pt-BR.json" -> "pt-BR"
+                var code = resource[prefix.Length..^5];
+
+                // Skip the base language file — en-US is added explicitly below
+                if (code.Equals(DefaultCulture, StringComparison.OrdinalIgnoreCase))
+                {
+                    continue;
+                }
+
+                var displayName = GetDisplayName(code);
+                options.Add(new LocalizationOption(displayName, code));
+            }
+
+            // Ensure en-US is always present
+            options.Add(new LocalizationOption("English", DefaultCulture));
+
+            options.Sort((a, b) => string.Compare(a.Name, b.Name, StringComparison.OrdinalIgnoreCase));
+            return options;
+        }
+
+        private static string GetDisplayName(string cultureCode)
+        {
+            // Handle Jellyfin-specific codes that aren't valid CultureInfo names
+            if (Bcp47ToJellyfinMap.Values.Contains(cultureCode))
+            {
+                // Convert underscore to hyphen for CultureInfo lookup
+                var normalized = cultureCode.Replace('_', '-');
+                try
+                {
+                    return CultureInfo.GetCultureInfo(normalized).NativeName;
+                }
+                catch (CultureNotFoundException)
+                {
+                    return cultureCode;
+                }
+            }
+
+            try
+            {
+                return CultureInfo.GetCultureInfo(cultureCode).NativeName;
+            }
+            catch (CultureNotFoundException)
+            {
+                // Custom/novelty codes like "pr" (Pirate) — fall back to code itself
+                return cultureCode;
+            }
         }
 
         /// <inheritdoc />
diff --git a/Jellyfin.Api/Controllers/LibraryController.cs b/Jellyfin.Api/Controllers/LibraryController.cs
index 69c17f2486..0839d62a5c 100644
--- a/Jellyfin.Api/Controllers/LibraryController.cs
+++ b/Jellyfin.Api/Controllers/LibraryController.cs
@@ -935,11 +935,11 @@ public class LibraryController : BaseJellyfinApiController
         try
         {
             await _activityManager.CreateAsync(new ActivityLog(
-                string.Format(CultureInfo.InvariantCulture, _localization.GetLocalizedString("UserDownloadingItemWithValues"), user.Username, item.Name),
+                string.Format(CultureInfo.InvariantCulture, _localization.GetServerLocalizedString("UserDownloadingItemWithValues"), user.Username, item.Name),
                 "UserDownloadingContent",
                 User.GetUserId())
             {
-                ShortOverview = string.Format(CultureInfo.InvariantCulture, _localization.GetLocalizedString("AppDeviceValues"), User.GetClient(), User.GetDevice()),
+                ShortOverview = string.Format(CultureInfo.InvariantCulture, _localization.GetServerLocalizedString("AppDeviceValues"), User.GetClient(), User.GetDevice()),
                 ItemId = item.Id.ToString("N", CultureInfo.InvariantCulture)
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Library/LyricDownloadFailureLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Library/LyricDownloadFailureLogger.cs
index 5f4864e953..cfd1cbe05b 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Library/LyricDownloadFailureLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Library/LyricDownloadFailureLogger.cs
@@ -37,7 +37,7 @@ public class LyricDownloadFailureLogger : IEventConsumer<LyricDownloadFailureEve
         await _activityManager.CreateAsync(new ActivityLog(
             string.Format(
                 CultureInfo.InvariantCulture,
-                _localizationManager.GetLocalizedString("LyricDownloadFailureFromForItem"),
+                _localizationManager.GetServerLocalizedString("LyricDownloadFailureFromForItem"),
                 eventArgs.Provider,
                 GetItemName(eventArgs.Item)),
             "LyricDownloadFailure",
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Library/SubtitleDownloadFailureLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Library/SubtitleDownloadFailureLogger.cs
index 8fe380e4f4..24146210c6 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Library/SubtitleDownloadFailureLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Library/SubtitleDownloadFailureLogger.cs
@@ -37,7 +37,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Library
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("SubtitleDownloadFailureFromForItem"),
+                    _localizationManager.GetServerLocalizedString("SubtitleDownloadFailureFromForItem"),
                     eventArgs.Provider,
                     GetItemName(eventArgs.Item)),
                 "SubtitleDownloadFailure",
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationFailedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationFailedLogger.cs
index 1a8931a6dc..df526977a2 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationFailedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationFailedLogger.cs
@@ -35,7 +35,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Security
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("FailedLoginAttemptWithUserName"),
+                    _localizationManager.GetServerLocalizedString("FailedLoginAttemptWithUserName"),
                     eventArgs.Username),
                 "AuthenticationFailed",
                 Guid.Empty)
@@ -43,7 +43,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Security
                 LogSeverity = LogLevel.Error,
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("LabelIpAddressValue"),
+                    _localizationManager.GetServerLocalizedString("LabelIpAddressValue"),
                     eventArgs.RemoteEndPoint),
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationSucceededLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationSucceededLogger.cs
index 584d559e44..fa9ce21170 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationSucceededLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Security/AuthenticationSucceededLogger.cs
@@ -33,14 +33,14 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Security
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("AuthenticationSucceededWithUserName"),
+                    _localizationManager.GetServerLocalizedString("AuthenticationSucceededWithUserName"),
                     eventArgs.User.Name),
                 "AuthenticationSucceeded",
                 eventArgs.User.Id)
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("LabelIpAddressValue"),
+                    _localizationManager.GetServerLocalizedString("LabelIpAddressValue"),
                     eventArgs.SessionInfo?.RemoteEndPoint),
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStartLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStartLogger.cs
index 73323acb37..8f71966b83 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStartLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStartLogger.cs
@@ -61,7 +61,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("UserStartedPlayingItemWithValues"),
+                    _localizationManager.GetServerLocalizedString("UserStartedPlayingItemWithValues"),
                     user.Username,
                     GetItemName(eventArgs.MediaInfo),
                     eventArgs.DeviceName),
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStopLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStopLogger.cs
index b75567539c..09d68e4451 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStopLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Session/PlaybackStopLogger.cs
@@ -69,7 +69,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             await _activityManager.CreateAsync(new ActivityLog(
                     string.Format(
                         CultureInfo.InvariantCulture,
-                        _localizationManager.GetLocalizedString("UserStoppedPlayingItemWithValues"),
+                        _localizationManager.GetServerLocalizedString("UserStoppedPlayingItemWithValues"),
                         user.Username,
                         GetItemName(item),
                         eventArgs.DeviceName),
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionEndedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionEndedLogger.cs
index b90708a2f2..74dfeebba6 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionEndedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionEndedLogger.cs
@@ -38,7 +38,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("UserOfflineFromDevice"),
+                    _localizationManager.GetServerLocalizedString("UserOfflineFromDevice"),
                     eventArgs.Argument.UserName,
                     eventArgs.Argument.DeviceName),
                 "SessionEnded",
@@ -46,7 +46,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("LabelIpAddressValue"),
+                    _localizationManager.GetServerLocalizedString("LabelIpAddressValue"),
                     eventArgs.Argument.RemoteEndPoint),
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionStartedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionStartedLogger.cs
index 139c2e2acb..4028522838 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionStartedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Session/SessionStartedLogger.cs
@@ -38,7 +38,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("UserOnlineFromDevice"),
+                    _localizationManager.GetServerLocalizedString("UserOnlineFromDevice"),
                     eventArgs.Argument.UserName,
                     eventArgs.Argument.DeviceName),
                 "SessionStarted",
@@ -46,7 +46,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Session
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("LabelIpAddressValue"),
+                    _localizationManager.GetServerLocalizedString("LabelIpAddressValue"),
                     eventArgs.Argument.RemoteEndPoint)
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/System/TaskCompletedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/System/TaskCompletedLogger.cs
index da82a3b30f..1e3dc7c92e 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/System/TaskCompletedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/System/TaskCompletedLogger.cs
@@ -47,7 +47,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.System
             var time = result.EndTimeUtc - result.StartTimeUtc;
             var runningTime = string.Format(
                 CultureInfo.InvariantCulture,
-                _localizationManager.GetLocalizedString("LabelRunningTimeValue"),
+                _localizationManager.GetServerLocalizedString("LabelRunningTimeValue"),
                 ToUserFriendlyString(time));
 
             if (result.Status == TaskCompletionStatus.Failed)
@@ -65,7 +65,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.System
                 }
 
                 await _activityManager.CreateAsync(new ActivityLog(
-                    string.Format(CultureInfo.InvariantCulture, _localizationManager.GetLocalizedString("ScheduledTaskFailedWithName"), task.Name),
+                    string.Format(CultureInfo.InvariantCulture, _localizationManager.GetServerLocalizedString("ScheduledTaskFailedWithName"), task.Name),
                     NotificationType.TaskFailed.ToString(),
                     Guid.Empty)
                 {
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstallationFailedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstallationFailedLogger.cs
index 632f30c7ad..9fb007aca7 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstallationFailedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstallationFailedLogger.cs
@@ -35,14 +35,14 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Updates
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("NameInstallFailed"),
+                    _localizationManager.GetServerLocalizedString("NameInstallFailed"),
                     eventArgs.InstallationInfo.Name),
                 NotificationType.InstallationFailed.ToString(),
                 Guid.Empty)
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("VersionNumber"),
+                    _localizationManager.GetServerLocalizedString("VersionNumber"),
                     eventArgs.InstallationInfo.Version),
                 Overview = eventArgs.Exception.Message
             }).ConfigureAwait(false);
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstalledLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstalledLogger.cs
index 4b49b714cf..2aa738c153 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstalledLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginInstalledLogger.cs
@@ -35,14 +35,14 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Updates
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("PluginInstalledWithName"),
+                    _localizationManager.GetServerLocalizedString("PluginInstalledWithName"),
                     eventArgs.Argument.Name),
                 NotificationType.PluginInstalled.ToString(),
                 Guid.Empty)
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("VersionNumber"),
+                    _localizationManager.GetServerLocalizedString("VersionNumber"),
                     eventArgs.Argument.Version)
             }).ConfigureAwait(false);
         }
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUninstalledLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUninstalledLogger.cs
index 2d24de7fc6..f7e651173d 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUninstalledLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUninstalledLogger.cs
@@ -35,7 +35,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Updates
             await _activityManager.CreateAsync(new ActivityLog(
                     string.Format(
                         CultureInfo.InvariantCulture,
-                        _localizationManager.GetLocalizedString("PluginUninstalledWithName"),
+                        _localizationManager.GetServerLocalizedString("PluginUninstalledWithName"),
                         eventArgs.Argument.Name),
                     NotificationType.PluginUninstalled.ToString(),
                     Guid.Empty))
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUpdatedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUpdatedLogger.cs
index e892d3dd9a..bca9662839 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUpdatedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Updates/PluginUpdatedLogger.cs
@@ -35,14 +35,14 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Updates
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("PluginUpdatedWithName"),
+                    _localizationManager.GetServerLocalizedString("PluginUpdatedWithName"),
                     eventArgs.Argument.Name),
                 NotificationType.PluginUpdateInstalled.ToString(),
                 Guid.Empty)
             {
                 ShortOverview = string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("VersionNumber"),
+                    _localizationManager.GetServerLocalizedString("VersionNumber"),
                     eventArgs.Argument.Version),
                 Overview = eventArgs.Argument.Changelog
             }).ConfigureAwait(false);
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserCreatedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserCreatedLogger.cs
index 4f063f6a1b..cf5c81b981 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserCreatedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserCreatedLogger.cs
@@ -33,7 +33,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Users
             await _activityManager.CreateAsync(new ActivityLog(
                     string.Format(
                         CultureInfo.InvariantCulture,
-                        _localizationManager.GetLocalizedString("UserCreatedWithName"),
+                        _localizationManager.GetServerLocalizedString("UserCreatedWithName"),
                         eventArgs.Argument.Username),
                     "UserCreated",
                     eventArgs.Argument.Id))
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserDeletedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserDeletedLogger.cs
index ba4a072e84..720480c28f 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserDeletedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserDeletedLogger.cs
@@ -34,7 +34,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Users
             await _activityManager.CreateAsync(new ActivityLog(
                     string.Format(
                         CultureInfo.InvariantCulture,
-                        _localizationManager.GetLocalizedString("UserDeletedWithName"),
+                        _localizationManager.GetServerLocalizedString("UserDeletedWithName"),
                         eventArgs.Argument.Username),
                     "UserDeleted",
                     Guid.Empty))
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserLockedOutLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserLockedOutLogger.cs
index bbc00567d1..efaf19397f 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserLockedOutLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserLockedOutLogger.cs
@@ -35,7 +35,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Users
             await _activityManager.CreateAsync(new ActivityLog(
                 string.Format(
                     CultureInfo.InvariantCulture,
-                    _localizationManager.GetLocalizedString("UserLockedOutWithName"),
+                    _localizationManager.GetServerLocalizedString("UserLockedOutWithName"),
                     eventArgs.Argument.Username),
                 NotificationType.UserLockedOut.ToString(),
                 eventArgs.Argument.Id)
diff --git a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserPasswordChangedLogger.cs b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserPasswordChangedLogger.cs
index 7219704ec6..cc9efa7061 100644
--- a/Jellyfin.Server.Implementations/Events/Consumers/Users/UserPasswordChangedLogger.cs
+++ b/Jellyfin.Server.Implementations/Events/Consumers/Users/UserPasswordChangedLogger.cs
@@ -33,7 +33,7 @@ namespace Jellyfin.Server.Implementations.Events.Consumers.Users
             await _activityManager.CreateAsync(new ActivityLog(
                     string.Format(
                         CultureInfo.InvariantCulture,
-                        _localizationManager.GetLocalizedString("UserPasswordChangedWithName"),
+                        _localizationManager.GetServerLocalizedString("UserPasswordChangedWithName"),
                         eventArgs.Argument.Username),
                     "UserPasswordChanged",
                     eventArgs.Argument.Id))
diff --git a/Jellyfin.Server/Middleware/AcceptLanguageMiddleware.cs b/Jellyfin.Server/Middleware/AcceptLanguageMiddleware.cs
new file mode 100644
index 0000000000..57390ae005
--- /dev/null
+++ b/Jellyfin.Server/Middleware/AcceptLanguageMiddleware.cs
@@ -0,0 +1,137 @@
+using System;
+using System.Collections.Generic;
+using System.Globalization;
+using System.Linq;
+using System.Threading.Tasks;
+using Emby.Server.Implementations.Localization;
+using MediaBrowser.Controller.Configuration;
+using Microsoft.AspNetCore.Http;
+
+namespace Jellyfin.Server.Middleware;
+
+/// <summary>
+/// Middleware that resolves the <c>Accept-Language</c> request header
+/// to an ordered list of Jellyfin-supported cultures, sets the fallback chain
+/// on <see cref="LocalizationManager.RequestCultureFallback"/>, and writes
+/// the <c>Content-Language</c> response header.
+/// </summary>
+public class AcceptLanguageMiddleware
+{
+    private readonly RequestDelegate _next;
+
+    /// <summary>
+    /// Initializes a new instance of the <see cref="AcceptLanguageMiddleware"/> class.
+    /// </summary>
+    /// <param name="next">Next request delegate.</param>
+    public AcceptLanguageMiddleware(RequestDelegate next)
+    {
+        _next = next;
+    }
+
+    /// <summary>
+    /// Invoke request.
+    /// </summary>
+    /// <param name="context">Request context.</param>
+    /// <param name="configurationManager">The server configuration manager.</param>
+    /// <returns>Task.</returns>
+    public async Task Invoke(HttpContext context, IServerConfigurationManager configurationManager)
+    {
+        var chain = ResolveLanguages(context.Request, configurationManager);
+        if (chain is not null)
+        {
+            LocalizationManager.RequestCultureFallback = chain;
+            CultureInfo.CurrentUICulture = CultureInfo.GetCultureInfo(chain[0]);
+        }
+
+        context.Response.OnStarting(
+            static state =>
+            {
+                var (ctx, languages) = ((HttpContext, IReadOnlyList<string>?))state;
+                if (languages is not null)
+                {
+                    ctx.Response.Headers.ContentLanguage = string.Join(", ", languages);
+                }
+                else
+                {
+                    var culture = CultureInfo.CurrentUICulture.Name;
+                    if (!string.IsNullOrEmpty(culture))
+                    {
+                        ctx.Response.Headers.ContentLanguage = culture;
+                    }
+                }
+
+                return Task.CompletedTask;
+            },
+            (context, chain));
+
+        try
+        {
+            await _next(context).ConfigureAwait(false);
+        }
+        finally
+        {
+            LocalizationManager.RequestCultureFallback = null;
+        }
+    }
+
+    private static IReadOnlyList<string>? ResolveLanguages(HttpRequest request, IServerConfigurationManager configurationManager)
+    {
+        var acceptLanguageHeader = request.GetTypedHeaders().AcceptLanguage;
+        if (acceptLanguageHeader is null || acceptLanguageHeader.Count == 0)
+        {
+            return null;
+        }
+
+        var languages = acceptLanguageHeader
+            .OrderByDescending(h => h.Quality ?? 1)
+            .Select(h => h.Value.ToString());
+
+        var chain = new List<string>();
+        var seen = new HashSet<string>(StringComparer.OrdinalIgnoreCase);
+
+        foreach (var lang in languages)
+        {
+            TryAddCulture(lang, chain, seen);
+        }
+
+        // Append server default culture if not already present
+        var serverCulture = configurationManager.Configuration.UICulture;
+        if (!string.IsNullOrEmpty(serverCulture))
+        {
+            TryAddCulture(serverCulture, chain, seen);
+        }
+
+        // Ensure en-US is always the final fallback
+        TryAddCulture("en-US", chain, seen);
+
+        return chain;
+    }
+
+    private static void TryAddCulture(string lang, List<string> chain, HashSet<string> seen)
+    {
+        // Direct match
+        if (LocalizationManager.HasTranslation(lang) && seen.Add(lang))
+        {
+            chain.Add(lang);
+            return;
+        }
+
+        // BCP-47 to Jellyfin underscore mapping (e.g. es-419 -> es_419)
+        if (LocalizationManager.Bcp47ToJellyfinMap.TryGetValue(lang, out var mapped) && seen.Add(mapped))
+        {
+            chain.Add(mapped);
+            return;
+        }
+
+        // Parent culture fallback (e.g. de-DE -> de)
+        var dashIndex = lang.IndexOf('-', StringComparison.Ordinal);
+        if (dashIndex > 0)
+        {
+            var parent = lang[..dashIndex];
+            if (LocalizationManager.HasTranslation(parent) && seen.Add(parent))
+            {
+                chain.Add(parent);
+            }
+        }
+    }
+}
diff --git a/Jellyfin.Server/Startup.cs b/Jellyfin.Server/Startup.cs
index f6a4ae7d6e..ea677cf6d9 100644
--- a/Jellyfin.Server/Startup.cs
+++ b/Jellyfin.Server/Startup.cs
@@ -1,4 +1,5 @@
 using System;
+using System.Globalization;
 using System.IO;
 using System.Net;
 using System.Net.Http;
@@ -16,6 +17,7 @@ using Jellyfin.Networking.HappyEyeballs;
 using Jellyfin.Server.Extensions;
 using Jellyfin.Server.HealthChecks;
 using Jellyfin.Server.Implementations.Extensions;
+using Jellyfin.Server.Middleware;
 using MediaBrowser.Common.Net;
 using MediaBrowser.Controller.Configuration;
 using MediaBrowser.Controller.Extensions;
@@ -127,6 +129,14 @@ namespace Jellyfin.Server
             services.AddHlsPlaylistGenerator();
             services.AddLiveTvServices();
 
+            var serverUICulture = _serverConfigurationManager.Configuration.UICulture;
+            if (string.IsNullOrEmpty(serverUICulture))
+            {
+                serverUICulture = "en-US";
+            }
+
+            CultureInfo.DefaultThreadCurrentUICulture = new CultureInfo(serverUICulture);
+
             services.AddHostedService<RecordingsHost>();
             services.AddHostedService<AutoDiscoveryHost>();
             services.AddHostedService<NfoUserDataSaver>();
@@ -168,6 +178,8 @@ namespace Jellyfin.Server
 
                 mainApp.UseCors();
 
+                mainApp.UseMiddleware<AcceptLanguageMiddleware>();
+
                 if (config.RequireHttps && _serverApplicationHost.ListenWithHttps)
                 {
                     mainApp.UseHttpsRedirection();
diff --git a/MediaBrowser.Controller/Net/BasePeriodicWebSocketListener.cs b/MediaBrowser.Controller/Net/BasePeriodicWebSocketListener.cs
index 6b1eac8047..2bcce168cf 100644
--- a/MediaBrowser.Controller/Net/BasePeriodicWebSocketListener.cs
+++ b/MediaBrowser.Controller/Net/BasePeriodicWebSocketListener.cs
@@ -209,6 +209,11 @@ namespace MediaBrowser.Controller.Net
                 var (connection, cts, state) = tuple;
                 var cancellationToken = cts.Token;
 
+                // Restore the culture context captured when the connection was established
+                // so that GetDataToSendForConnection produces a localized payload matching
+                // the client's Accept-Language preference rather than the server default.
+                connection.ApplyRequestCulture();
+
                 var data = await GetDataToSendForConnection(connection).ConfigureAwait(false);
                 if (data is null)
                 {
diff --git a/MediaBrowser.Controller/Net/IWebSocketConnection.cs b/MediaBrowser.Controller/Net/IWebSocketConnection.cs
index bdc0f9a10f..48431e75c3 100644
--- a/MediaBrowser.Controller/Net/IWebSocketConnection.cs
+++ b/MediaBrowser.Controller/Net/IWebSocketConnection.cs
@@ -77,5 +77,14 @@ namespace MediaBrowser.Controller.Net
         /// <param name="cancellationToken">The cancellation token.</param>
         /// <returns>Task.</returns>
         Task ReceiveAsync(CancellationToken cancellationToken = default);
+
+        /// <summary>
+        /// Applies the culture context captured when the connection was established
+        /// (from the upgrade request's <c>Accept-Language</c> header) to the current
+        /// async flow. Server-initiated message senders should call this before
+        /// localising any payload so that the response uses the client's preferred
+        /// language rather than the server default.
+        /// </summary>
+        void ApplyRequestCulture();
     }
 }
diff --git a/MediaBrowser.Model/Globalization/ILocalizationManager.cs b/MediaBrowser.Model/Globalization/ILocalizationManager.cs
index f6e65028e4..7ad240abfb 100644
--- a/MediaBrowser.Model/Globalization/ILocalizationManager.cs
+++ b/MediaBrowser.Model/Globalization/ILocalizationManager.cs
@@ -50,6 +50,15 @@ public interface ILocalizationManager
     /// <returns>System.String.</returns>
     string GetLocalizedString(string phrase);
 
+    /// <summary>
+    /// Gets the localized string using the server's configured UICulture,
+    /// ignoring the current request's culture. Use this for data that is
+    /// persisted (e.g. activity log entries) rather than returned per-request.
+    /// </summary>
+    /// <param name="phrase">The phrase.</param>
+    /// <returns>System.String.</returns>
+    string GetServerLocalizedString(string phrase);
+
     /// <summary>
     /// Gets the localization options.
     /// </summary>
diff --git a/tests/Jellyfin.Server.Implementations.Tests/Localization/LocalizationManagerTests.cs b/tests/Jellyfin.Server.Implementations.Tests/Localization/LocalizationManagerTests.cs
index acabaf3acb..1c4d0d4a8a 100644
--- a/tests/Jellyfin.Server.Implementations.Tests/Localization/LocalizationManagerTests.cs
+++ b/tests/Jellyfin.Server.Implementations.Tests/Localization/LocalizationManagerTests.cs
@@ -1,4 +1,5 @@
 using System;
+using System.Globalization;
 using System.Linq;
 using System.Threading.Tasks;
 using BitFaster.Caching;
@@ -305,6 +306,166 @@ namespace Jellyfin.Server.Implementations.Tests.Localization
             Assert.Equal(key, translated);
         }
 
+        [Fact]
+        public void GetLocalizedString_WithCulture_ReturnsTranslation()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            var translated = localizationManager.GetLocalizedString("Artists", "de");
+            Assert.Equal("Interpreten", translated);
+        }
+
+        [Fact]
+        public void GetLocalizedString_WithCulture_FallsBackToEnUs()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            // A culture with no translation file should fall back to en-US
+            var translated = localizationManager.GetLocalizedString("Artists", "zz");
+            Assert.Equal("Artists", translated);
+        }
+
+        [Fact]
+        public void GetLocalizedString_WithBcp47Normalization_ReturnsTranslation()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            // es-419 is stored as es_419 in Jellyfin
+            var translated = localizationManager.GetLocalizedString("Default", "es-419");
+            Assert.NotEqual("Default", translated);
+        }
+
+        [Fact]
+        public void GetServerLocalizedString_UsesServerCulture()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "de"
+            });
+
+            // Even if CurrentUICulture is fr, GetServerLocalizedString should use the server's "de"
+            var previousCulture = CultureInfo.CurrentUICulture;
+            try
+            {
+                CultureInfo.CurrentUICulture = CultureInfo.GetCultureInfo("fr");
+                var translated = localizationManager.GetServerLocalizedString("Artists");
+                Assert.Equal("Interpreten", translated);
+            }
+            finally
+            {
+                CultureInfo.CurrentUICulture = previousCulture;
+            }
+        }
+
+        [Fact]
+        public void GetLocalizedString_FallbackChain_UsesFirstAvailableCulture()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            // Set fallback chain: de -> fr -> en-US
+            // "Artists" exists in de as "Interpreten", should use de (first in chain)
+            LocalizationManager.RequestCultureFallback = new[] { "de", "fr", "en-US" };
+            try
+            {
+                var translated = localizationManager.GetLocalizedString("Artists");
+                Assert.Equal("Interpreten", translated);
+            }
+            finally
+            {
+                LocalizationManager.RequestCultureFallback = null;
+            }
+        }
+
+        [Fact]
+        public void GetLocalizedString_FallbackChain_SkipsMissingAndUsesNext()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            // "zz" has no translation file so the key won't be found there,
+            // should fall through to de which has "Artists" as "Interpreten"
+            LocalizationManager.RequestCultureFallback = new[] { "zz", "de", "en-US" };
+            try
+            {
+                var translated = localizationManager.GetLocalizedString("Artists");
+                Assert.Equal("Interpreten", translated);
+            }
+            finally
+            {
+                LocalizationManager.RequestCultureFallback = null;
+            }
+        }
+
+        [Fact]
+        public void GetLocalizedString_FallbackChain_ReturnsKeyWhenNoTranslation()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            var key = "CompletelyNonExistentKey";
+            LocalizationManager.RequestCultureFallback = new[] { "de", "en-US" };
+            try
+            {
+                var translated = localizationManager.GetLocalizedString(key);
+                Assert.Equal(key, translated);
+            }
+            finally
+            {
+                LocalizationManager.RequestCultureFallback = null;
+            }
+        }
+
+        [Fact]
+        public void GetLocalizedString_NoFallbackChain_UsesCurrentUICulture()
+        {
+            var localizationManager = Setup(new ServerConfiguration
+            {
+                UICulture = "en-US"
+            });
+
+            var previousCulture = CultureInfo.CurrentUICulture;
+            try
+            {
+                CultureInfo.CurrentUICulture = CultureInfo.GetCultureInfo("de");
+                LocalizationManager.RequestCultureFallback = null;
+
+                var translated = localizationManager.GetLocalizedString("Artists");
+                Assert.Equal("Interpreten", translated);
+            }
+            finally
+            {
+                CultureInfo.CurrentUICulture = previousCulture;
+            }
+        }
+
+        [Theory]
+        [InlineData("de", true)]
+        [InlineData("en-US", true)]
+        [InlineData("fr", true)]
+        [InlineData("es_419", true)]
+        [InlineData("nonexistent", false)]
+        [InlineData("zz-ZZ", false)]
+        public void HasTranslation_ReturnsExpected(string culture, bool expected)
+        {
+            Assert.Equal(expected, LocalizationManager.HasTranslation(culture));
+        }
+
         private LocalizationManager Setup(ServerConfiguration config)
         {
             var mockConfiguration = new Mock<IServerConfigurationManager>();