diff --git a/Emby.Server.Implementations/ApplicationHost.cs b/Emby.Server.Implementations/ApplicationHost.cs
index 1f11bdad74..6fd152a42d 100644
--- a/Emby.Server.Implementations/ApplicationHost.cs
+++ b/Emby.Server.Implementations/ApplicationHost.cs
@@ -1067,9 +1067,9 @@ namespace Emby.Server.Implementations
         /// <summary>
         /// Gets the system status.
         /// </summary>
-        /// <param name="source">Where this request originated.</param>
+        /// <param name="request">Where this request originated.</param>
         /// <returns>SystemInfo.</returns>
-        public SystemInfo GetSystemInfo(IPAddress source)
+        public SystemInfo GetSystemInfo(HttpRequest request)
         {
             return new SystemInfo
             {
@@ -1091,7 +1091,7 @@ namespace Emby.Server.Implementations
                 CanLaunchWebBrowser = CanLaunchWebBrowser,
                 TranscodingTempPath = ConfigurationManager.GetTranscodePath(),
                 ServerName = FriendlyName,
-                LocalAddress = GetSmartApiUrl(source),
+                LocalAddress = GetSmartApiUrl(request),
                 SupportsLibraryMonitor = true,
                 SystemArchitecture = RuntimeInformation.OSArchitecture,
                 PackageName = _startupOptions.PackageName
@@ -1103,7 +1103,7 @@ namespace Emby.Server.Implementations
                 .Select(i => new WakeOnLanInfo(i))
                 .ToList();
 
-        public PublicSystemInfo GetPublicSystemInfo(IPAddress address)
+        public PublicSystemInfo GetPublicSystemInfo(HttpRequest request)
         {
             return new PublicSystemInfo
             {
@@ -1112,7 +1112,7 @@ namespace Emby.Server.Implementations
                 Id = SystemId,
                 OperatingSystem = MediaBrowser.Common.System.OperatingSystem.Id.ToString(),
                 ServerName = FriendlyName,
-                LocalAddress = GetSmartApiUrl(address),
+                LocalAddress = GetSmartApiUrl(request),
                 StartupWizardCompleted = ConfigurationManager.CommonConfiguration.IsStartupWizardCompleted
             };
         }
@@ -1140,6 +1140,18 @@ namespace Emby.Server.Implementations
         /// <inheritdoc/>
         public string GetSmartApiUrl(HttpRequest request, int? port = null)
         {
+            // Return the host in the HTTP request as the API url
+            if (ConfigurationManager.GetNetworkConfiguration().EnablePublishedServerUriByRequest)
+            {
+                int? requestPort = request.Host.Port;
+                if ((requestPort == 80 && string.Equals(request.Scheme, "http", StringComparison.OrdinalIgnoreCase)) || (requestPort == 443 && string.Equals(request.Scheme, "https", StringComparison.OrdinalIgnoreCase)))
+                {
+                    requestPort = -1;
+                }
+
+                return GetLocalApiUrl(request.Host.Host, request.Scheme, requestPort);
+            }
+
             // Published server ends with a /
             if (!string.IsNullOrEmpty(PublishedServerUrl))
             {
diff --git a/Jellyfin.Api/Controllers/SystemController.cs b/Jellyfin.Api/Controllers/SystemController.cs
index 741bdfee97..904738bb45 100644
--- a/Jellyfin.Api/Controllers/SystemController.cs
+++ b/Jellyfin.Api/Controllers/SystemController.cs
@@ -66,7 +66,7 @@ namespace Jellyfin.Api.Controllers
         [ProducesResponseType(StatusCodes.Status200OK)]
         public ActionResult<SystemInfo> GetSystemInfo()
         {
-            return _appHost.GetSystemInfo(Request.HttpContext.Connection.RemoteIpAddress ?? IPAddress.Loopback);
+            return _appHost.GetSystemInfo(Request);
         }
 
         /// <summary>
@@ -78,7 +78,7 @@ namespace Jellyfin.Api.Controllers
         [ProducesResponseType(StatusCodes.Status200OK)]
         public ActionResult<PublicSystemInfo> GetPublicSystemInfo()
         {
-            return _appHost.GetPublicSystemInfo(Request.HttpContext.Connection.RemoteIpAddress ?? IPAddress.Loopback);
+            return _appHost.GetPublicSystemInfo(Request);
         }
 
         /// <summary>
diff --git a/Jellyfin.Networking/Configuration/NetworkConfiguration.cs b/Jellyfin.Networking/Configuration/NetworkConfiguration.cs
index faf814c060..61db223d92 100644
--- a/Jellyfin.Networking/Configuration/NetworkConfiguration.cs
+++ b/Jellyfin.Networking/Configuration/NetworkConfiguration.cs
@@ -226,5 +226,10 @@ namespace Jellyfin.Networking.Configuration
         /// Gets or sets the known proxies. If the proxy is a network, it's added to the KnownNetworks.
         /// </summary>
         public string[] KnownProxies { get; set; } = Array.Empty<string>();
+
+        /// <summary>
+        /// Gets or sets a value indicating whether the published server uri is based on information in HTTP requests.
+        /// </summary>
+        public bool EnablePublishedServerUriByRequest { get; set; } = false;
     }
 }
diff --git a/Jellyfin.Server/Extensions/ApiServiceCollectionExtensions.cs b/Jellyfin.Server/Extensions/ApiServiceCollectionExtensions.cs
index 183480487a..867f79b6b0 100644
--- a/Jellyfin.Server/Extensions/ApiServiceCollectionExtensions.cs
+++ b/Jellyfin.Server/Extensions/ApiServiceCollectionExtensions.cs
@@ -188,7 +188,8 @@ namespace Jellyfin.Server.Extensions
                     // https://github.com/dotnet/aspnetcore/blob/master/src/Middleware/HttpOverrides/src/ForwardedHeadersMiddleware.cs
                     // Enable debug logging on Microsoft.AspNetCore.HttpOverrides.ForwardedHeadersMiddleware to help investigate issues.
 
-                    options.ForwardedHeaders = ForwardedHeaders.XForwardedFor | ForwardedHeaders.XForwardedProto;
+                    options.ForwardedHeaders = ForwardedHeaders.XForwardedFor | ForwardedHeaders.XForwardedProto | ForwardedHeaders.XForwardedHost;
+
                     if (config.KnownProxies.Length == 0)
                     {
                         options.KnownNetworks.Clear();
diff --git a/MediaBrowser.Controller/IServerApplicationHost.cs b/MediaBrowser.Controller/IServerApplicationHost.cs
index 3da0a58753..7e5e742f5d 100644
--- a/MediaBrowser.Controller/IServerApplicationHost.cs
+++ b/MediaBrowser.Controller/IServerApplicationHost.cs
@@ -50,11 +50,11 @@ namespace MediaBrowser.Controller
         /// <summary>
         /// Gets the system info.
         /// </summary>
-        /// <param name="source">The originator of the request.</param>
+        /// <param name="request">The HTTP request.</param>
         /// <returns>SystemInfo.</returns>
-        SystemInfo GetSystemInfo(IPAddress source);
+        SystemInfo GetSystemInfo(HttpRequest request);
 
-        PublicSystemInfo GetPublicSystemInfo(IPAddress address);
+        PublicSystemInfo GetPublicSystemInfo(HttpRequest request);
 
         /// <summary>
         /// Gets a URL specific for the request.