diff --git a/samples/HostedInAspNet.Client/HostedInAspNet.Client.csproj b/samples/HostedInAspNet.Client/HostedInAspNet.Client.csproj
index 038ec80f9f..fbec52a713 100644
--- a/samples/HostedInAspNet.Client/HostedInAspNet.Client.csproj
+++ b/samples/HostedInAspNet.Client/HostedInAspNet.Client.csproj
@@ -3,9 +3,6 @@
   <PropertyGroup>
     <TargetFramework>netstandard2.0</TargetFramework>
     <OutputType>Exe</OutputType>
-
-    <!-- Temporary workaround for a VS build issue -->
-    <BlazorRebuildOnFileChange>false</BlazorRebuildOnFileChange>
   </PropertyGroup>
 
   <ItemGroup>
diff --git a/src/Microsoft.AspNetCore.Blazor.Server/AutoRebuild/AutoRebuildExtensions.cs b/src/Microsoft.AspNetCore.Blazor.Server/AutoRebuild/AutoRebuildExtensions.cs
index a54e023966..471f6e9545 100644
--- a/src/Microsoft.AspNetCore.Blazor.Server/AutoRebuild/AutoRebuildExtensions.cs
+++ b/src/Microsoft.AspNetCore.Blazor.Server/AutoRebuild/AutoRebuildExtensions.cs
@@ -3,7 +3,10 @@
 
 using Microsoft.AspNetCore.Blazor.Server;
 using Microsoft.AspNetCore.Blazor.Server.AutoRebuild;
+using Microsoft.Extensions.DependencyInjection;
+using Microsoft.Extensions.Logging;
 using System;
+using System.Collections.Generic;
 using System.IO;
 using System.Linq;
 using System.Threading.Tasks;
@@ -19,7 +22,48 @@ namespace Microsoft.AspNetCore.Builder
         private static string[] _includedSuffixes = new[] { ".cs", ".cshtml", "index.html" };
         private static string[] _excludedDirectories = new[] { "obj", "bin" };
 
-        public static void UseAutoRebuild(this IApplicationBuilder appBuilder, BlazorConfig config)
+        // To ensure the FileSystemWatchers aren't collected, reference them
+        // in this static list. They never need to be removed because there's no
+        // way to remove middleware once it's registered.
+        private static List<object> _uncollectableWatchers = new List<object>();
+
+        public static void UseHostedAutoRebuild(this IApplicationBuilder appBuilder, BlazorConfig config, string hostAppContentRootPath)
+        {
+            var isFirstFileWrite = true;
+            WatchFileSystem(config, () =>
+            {
+                if (isFirstFileWrite)
+                {
+                    try
+                    {
+                        // Touch any .cs file to force the host project to rebuild
+                        // (which in turn rebuilds the client, since it's referenced)
+                        var fileToTouch = Directory.EnumerateFiles(
+                            hostAppContentRootPath,
+                            "*.cs",
+                            SearchOption.AllDirectories).FirstOrDefault();
+
+                        if (!string.IsNullOrEmpty(fileToTouch))
+                        {
+                            File.SetLastWriteTime(fileToTouch, DateTime.Now);
+                        }
+                    }
+                    catch (Exception ex)
+                    {
+                        // If we don't have permission to write these files, autorebuild will not be enabled
+                        var loggerFactory = appBuilder.ApplicationServices.GetRequiredService<ILoggerFactory>();
+                        var logger = loggerFactory.CreateLogger(typeof (AutoRebuildExtensions));
+                        logger?.LogWarning(ex,
+                            "Cannot autorebuild because there was an error when writing to a file in '{0}'.",
+                            hostAppContentRootPath);
+                    }
+
+                    isFirstFileWrite = false;
+                }
+            });
+        }
+
+        public static void UseDevServerAutoRebuild(this IApplicationBuilder appBuilder, BlazorConfig config)
         {
             // Currently this only supports VS for Windows. Later on we can add
             // an IRebuildService implementation for VS for Mac, etc.
@@ -91,6 +135,12 @@ namespace Microsoft.AspNetCore.Builder
             fsw.IncludeSubdirectories = true;
             fsw.EnableRaisingEvents = true;
 
+            // Ensure the watcher is not GCed for as long as the app lives
+            lock (_uncollectableWatchers)
+            {
+                _uncollectableWatchers.Add(fsw);
+            }
+
             void OnEvent(object sender, FileSystemEventArgs eventArgs)
             {
                 if (!File.Exists(eventArgs.FullPath))
diff --git a/src/Microsoft.AspNetCore.Blazor.Server/BlazorAppBuilderExtensions.cs b/src/Microsoft.AspNetCore.Blazor.Server/BlazorAppBuilderExtensions.cs
index 9c74a6176d..4bc987345c 100644
--- a/src/Microsoft.AspNetCore.Blazor.Server/BlazorAppBuilderExtensions.cs
+++ b/src/Microsoft.AspNetCore.Blazor.Server/BlazorAppBuilderExtensions.cs
@@ -8,6 +8,7 @@ using Microsoft.Extensions.FileProviders;
 using Microsoft.AspNetCore.Hosting;
 using Microsoft.Net.Http.Headers;
 using System.Net.Mime;
+using System;
 
 namespace Microsoft.AspNetCore.Builder
 {
@@ -16,6 +17,8 @@ namespace Microsoft.AspNetCore.Builder
     /// </summary>
     public static class BlazorAppBuilderExtensions
     {
+        const string DevServerApplicationName = "dotnet-blazor";
+
         /// <summary>
         /// Configures the middleware pipeline to work with Blazor.
         /// </summary>
@@ -54,7 +57,14 @@ namespace Microsoft.AspNetCore.Builder
 
             if (env.IsDevelopment() && config.EnableAutoRebuilding)
             {
-                applicationBuilder.UseAutoRebuild(config);
+                if (env.ApplicationName.Equals(DevServerApplicationName, StringComparison.OrdinalIgnoreCase))
+                {
+                    applicationBuilder.UseDevServerAutoRebuild(config);
+                }
+                else
+                {
+                    applicationBuilder.UseHostedAutoRebuild(config, env.ContentRootPath);
+                }
             }
 
             // First, match the request against files in the client app dist directory
diff --git a/src/Microsoft.AspNetCore.Blazor.Templates/content/BlazorHosted-CSharp/BlazorHosted-CSharp.Client/BlazorHosted-CSharp.Client.csproj b/src/Microsoft.AspNetCore.Blazor.Templates/content/BlazorHosted-CSharp/BlazorHosted-CSharp.Client/BlazorHosted-CSharp.Client.csproj
index 02613021e2..ff0f4e61aa 100644
--- a/src/Microsoft.AspNetCore.Blazor.Templates/content/BlazorHosted-CSharp/BlazorHosted-CSharp.Client/BlazorHosted-CSharp.Client.csproj
+++ b/src/Microsoft.AspNetCore.Blazor.Templates/content/BlazorHosted-CSharp/BlazorHosted-CSharp.Client/BlazorHosted-CSharp.Client.csproj
@@ -9,9 +9,6 @@
       https://dotnet.myget.org/f/blazor-dev/api/v3/index.json;
     </RestoreSources>
     <LangVersion>7.3</LangVersion>
-
-    <!-- Temporary workaround for a VS build issue -->
-    <BlazorRebuildOnFileChange>false</BlazorRebuildOnFileChange>
   </PropertyGroup>
 
   <ItemGroup>