diff --git a/Emby.Server.Implementations/AppBase/BaseApplicationPaths.cs b/Emby.Server.Implementations/AppBase/BaseApplicationPaths.cs
index 8bcd087452..bc47817438 100644
--- a/Emby.Server.Implementations/AppBase/BaseApplicationPaths.cs
+++ b/Emby.Server.Implementations/AppBase/BaseApplicationPaths.cs
@@ -1,8 +1,6 @@
 using System;
 using System.IO;
 using MediaBrowser.Common.Configuration;
-using MediaBrowser.Controller.Extensions;
-using Microsoft.Extensions.Configuration;
 
 namespace Emby.Server.Implementations.AppBase
 {
@@ -39,13 +37,7 @@ namespace Emby.Server.Implementations.AppBase
         /// <value>The program data path.</value>
         public string ProgramDataPath { get; }
 
-        /// <summary>
-        /// Gets the path to the web UI resources folder.
-        /// </summary>
-        /// <value>The web UI resources path.</value>
-        /// <remarks>
-        /// This value is not relevant if <see cref="ConfigurationExtensions.IsNoWebContent(IConfiguration)"/> is true.
-        /// </remarks>
+        /// <inheritdoc/>
         public string WebPath { get; }
 
         /// <summary>
diff --git a/Emby.Server.Implementations/ApplicationHost.cs b/Emby.Server.Implementations/ApplicationHost.cs
index 7262268a97..52c5176271 100644
--- a/Emby.Server.Implementations/ApplicationHost.cs
+++ b/Emby.Server.Implementations/ApplicationHost.cs
@@ -236,11 +236,6 @@ namespace Emby.Server.Implementations
         /// </summary>
         public int HttpsPort { get; private set; }
 
-        /// <summary>
-        /// Gets the content root for the webhost.
-        /// </summary>
-        public string ContentRoot { get; private set; }
-
         /// <summary>
         /// Gets the server configuration manager.
         /// </summary>
@@ -614,12 +609,6 @@ namespace Emby.Server.Implementations
             DiscoverTypes();
 
             await RegisterServices(serviceCollection, startupConfig).ConfigureAwait(false);
-
-            ContentRoot = ServerConfigurationManager.Configuration.DashboardSourcePath;
-            if (string.IsNullOrEmpty(ContentRoot))
-            {
-                ContentRoot = ServerConfigurationManager.ApplicationPaths.WebPath;
-            }
         }
 
         public async Task ExecuteWebsocketHandlerAsync(HttpContext context, Func<Task> next)
diff --git a/Jellyfin.Server/Program.cs b/Jellyfin.Server/Program.cs
index bfb2fc6b57..67251eb249 100644
--- a/Jellyfin.Server/Program.cs
+++ b/Jellyfin.Server/Program.cs
@@ -243,7 +243,7 @@ namespace Jellyfin.Server
             IConfiguration startupConfig,
             IApplicationPaths appPaths)
         {
-            var webhostBuilder = new WebHostBuilder()
+            return new WebHostBuilder()
                 .UseKestrel(options =>
                 {
                     var addresses = appHost.ServerConfigurationManager
@@ -289,24 +289,6 @@ namespace Jellyfin.Server
                     services.TryAdd(serviceCollection);
                 })
                 .UseStartup<Startup>();
-
-            // Set up static content hosting unless it has been disabled via config
-            if (!startupConfig.NoWebContent())
-            {
-                // Fail startup if the web content does not exist
-                if (!Directory.Exists(appHost.ContentRoot) || !Directory.GetFiles(appHost.ContentRoot).Any())
-                {
-                    throw new InvalidOperationException(
-                        "The server is expected to host web content, but the provided content directory is either " +
-                        $"invalid or empty: {appHost.ContentRoot}. If you do not want to host web content with the " +
-                        $"server, you may set the '{MediaBrowser.Controller.Extensions.ConfigurationExtensions.NoWebContentKey}' flag.");
-                }
-
-                // Configure the web host to host the static web content
-                webhostBuilder.UseContentRoot(appHost.ContentRoot);
-            }
-
-            return webhostBuilder;
         }
 
         /// <summary>
diff --git a/MediaBrowser.Common/Configuration/IApplicationPaths.cs b/MediaBrowser.Common/Configuration/IApplicationPaths.cs
index 5bdea7d8b3..870b90796c 100644
--- a/MediaBrowser.Common/Configuration/IApplicationPaths.cs
+++ b/MediaBrowser.Common/Configuration/IApplicationPaths.cs
@@ -1,3 +1,5 @@
+using MediaBrowser.Model.Configuration;
+
 namespace MediaBrowser.Common.Configuration
 {
     /// <summary>
@@ -12,9 +14,12 @@ namespace MediaBrowser.Common.Configuration
         string ProgramDataPath { get; }
 
         /// <summary>
-        /// Gets the path to the web UI resources folder
+        /// Gets the path to the web UI resources folder.
         /// </summary>
-        /// <value>The web UI resources path.</value>
+        /// <remarks>
+        /// This value is not relevant if the server is configured to not host any static web content. Additionally,
+        /// the value for <see cref="ServerConfiguration.DashboardSourcePath"/> takes precedence over this one.
+        /// </remarks>
         string WebPath { get; }
 
         /// <summary>
diff --git a/MediaBrowser.WebDashboard/Api/DashboardService.cs b/MediaBrowser.WebDashboard/Api/DashboardService.cs
index 11901c25fb..0114f5d602 100644
--- a/MediaBrowser.WebDashboard/Api/DashboardService.cs
+++ b/MediaBrowser.WebDashboard/Api/DashboardService.cs
@@ -136,6 +136,17 @@ namespace MediaBrowser.WebDashboard.Api
             _resultFactory = resultFactory;
             _resourceFileManager = resourceFileManager;
             _appConfig = appConfig;
+
+            // Validate web content path
+            string webContentPath = DashboardUIPath;
+            bool webContentPathValid = appConfig.NoWebContent() || (Directory.Exists(webContentPath) && Directory.GetFiles(webContentPath).Any());
+            if (!webContentPathValid)
+            {
+                throw new InvalidOperationException(
+                    "The server is expected to host web content, but the provided content directory is either " +
+                    $"invalid or empty: {webContentPath}. If you do not want to host web content with the server, " +
+                    $"you may set the '{Controller.Extensions.ConfigurationExtensions.NoWebContentKey}' flag.");
+            }
         }
 
         /// <summary>