diff --git a/src/Umbraco.Tests.Integration/TestServerTest/UmbracoTestServerTestBase.cs b/src/Umbraco.Tests.Integration/TestServerTest/UmbracoTestServerTestBase.cs
index 2434b2b8fb..1695c359bb 100644
--- a/src/Umbraco.Tests.Integration/TestServerTest/UmbracoTestServerTestBase.cs
+++ b/src/Umbraco.Tests.Integration/TestServerTest/UmbracoTestServerTestBase.cs
@@ -139,9 +139,10 @@ namespace Umbraco.Tests.Integration.TestServerTest
         public override void ConfigureServices(IServiceCollection services)
         {
             services.AddTransient<TestUmbracoDatabaseFactoryProvider>();
+            IWebHostEnvironment webHostEnvironment = TestHelper.GetWebHostEnvironment();
             TypeLoader typeLoader = services.AddTypeLoader(
                 GetType().Assembly,
-                TestHelper.GetWebHostEnvironment(),
+                webHostEnvironment,
                 TestHelper.GetHostingEnvironment(),
                 TestHelper.ConsoleLoggerFactory,
                 AppCaches.NoCache,
@@ -154,7 +155,7 @@ namespace Umbraco.Tests.Integration.TestServerTest
                 .AddConfiguration()
                 .AddUmbracoCore()
                 .AddWebComponents()
-                .AddRuntimeMinifier()
+                .AddRuntimeMinifier(webHostEnvironment)
                 .AddBackOfficeCore()
                 .AddBackOfficeAuthentication()
                 .AddBackOfficeIdentity()
diff --git a/src/Umbraco.Tests.Integration/Testing/UmbracoIntegrationTest.cs b/src/Umbraco.Tests.Integration/Testing/UmbracoIntegrationTest.cs
index 2a1e9a9298..cc56b250ac 100644
--- a/src/Umbraco.Tests.Integration/Testing/UmbracoIntegrationTest.cs
+++ b/src/Umbraco.Tests.Integration/Testing/UmbracoIntegrationTest.cs
@@ -215,7 +215,7 @@ namespace Umbraco.Tests.Integration.Testing
             builder.AddConfiguration()
                 .AddUmbracoCore()
                 .AddWebComponents()
-                .AddRuntimeMinifier()
+                .AddRuntimeMinifier(webHostEnvironment)
                 .AddBackOfficeAuthentication()
                 .AddBackOfficeIdentity()
                 .AddTestServices(TestHelper, GetAppCaches());
diff --git a/src/Umbraco.Web.BackOffice/DependencyInjection/UmbracoBuilderExtensions.cs b/src/Umbraco.Web.BackOffice/DependencyInjection/UmbracoBuilderExtensions.cs
index 6587f3c6e4..9cbcdf7054 100644
--- a/src/Umbraco.Web.BackOffice/DependencyInjection/UmbracoBuilderExtensions.cs
+++ b/src/Umbraco.Web.BackOffice/DependencyInjection/UmbracoBuilderExtensions.cs
@@ -20,6 +20,7 @@ using Umbraco.Web.BackOffice.Trees;
 using Umbraco.Web.Common.Authorization;
 using Umbraco.Web.Common.DependencyInjection;
 using Umbraco.Web.WebAssets;
+using IWebHostEnvironment = Microsoft.AspNetCore.Hosting.IWebHostEnvironment;
 
 namespace Umbraco.Web.BackOffice.DependencyInjection
 {
@@ -31,11 +32,11 @@ namespace Umbraco.Web.BackOffice.DependencyInjection
         /// <summary>
         /// Adds all required components to run the Umbraco back office
         /// </summary>
-        public static IUmbracoBuilder AddBackOffice(this IUmbracoBuilder builder) => builder
+        public static IUmbracoBuilder AddBackOffice(this IUmbracoBuilder builder, IWebHostEnvironment webHostEnvironment) => builder
                 .AddConfiguration()
                 .AddUmbracoCore()
                 .AddWebComponents()
-                .AddRuntimeMinifier()
+                .AddRuntimeMinifier(webHostEnvironment)
                 .AddBackOfficeCore()
                 .AddBackOfficeAuthentication()
                 .AddBackOfficeIdentity()
diff --git a/src/Umbraco.Web.Common/DependencyInjection/UmbracoBuilderExtensions.cs b/src/Umbraco.Web.Common/DependencyInjection/UmbracoBuilderExtensions.cs
index e8097335d6..7c64d4adbd 100644
--- a/src/Umbraco.Web.Common/DependencyInjection/UmbracoBuilderExtensions.cs
+++ b/src/Umbraco.Web.Common/DependencyInjection/UmbracoBuilderExtensions.cs
@@ -12,7 +12,9 @@ using Microsoft.AspNetCore.Server.Kestrel.Core;
 using Microsoft.Extensions.Configuration;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.Extensions.DependencyInjection.Extensions;
+using Microsoft.Extensions.FileProviders;
 using Microsoft.Extensions.Logging;
+using Microsoft.Extensions.Primitives;
 using Serilog;
 using Smidge;
 using Smidge.Nuglify;
@@ -207,9 +209,11 @@ namespace Umbraco.Web.Common.DependencyInjection
         /// <summary>
         /// Add runtime minifier support for Umbraco
         /// </summary>
-        public static IUmbracoBuilder AddRuntimeMinifier(this IUmbracoBuilder builder)
+        public static IUmbracoBuilder AddRuntimeMinifier(this IUmbracoBuilder builder, IWebHostEnvironment webHostEnvironment)
         {
-            builder.Services.AddSmidge(builder.Config.GetSection(Core.Constants.Configuration.ConfigRuntimeMinification));
+            var smidgePhysicalFileProvider = new SmidgePhysicalFileProvider(webHostEnvironment.ContentRootFileProvider, webHostEnvironment.WebRootFileProvider);
+
+            builder.Services.AddSmidge(builder.Config.GetSection(Core.Constants.Configuration.ConfigRuntimeMinification), smidgePhysicalFileProvider);
             builder.Services.AddSmidgeNuglify();
 
             return builder;
@@ -394,5 +398,29 @@ namespace Umbraco.Web.Common.DependencyInjection
 
             return new AspNetCoreHostingEnvironment(wrappedHostingSettings,wrappedWebRoutingSettings, webHostEnvironment);
         }
+
+        /// <summary>
+        /// This file provider lets us serve physical files to Smidge for minification from both wwwroot and App_Plugins (which is outside wwwroot).
+        /// This file provider is NOT intended for use anywhere else, as it exposes files from the content root.
+        /// </summary>
+        private class SmidgePhysicalFileProvider : IFileProvider
+        {
+            private readonly IFileProvider _contentRootFileProvider;
+            private readonly IFileProvider _webRooFileProvider;
+
+            public SmidgePhysicalFileProvider(IFileProvider contentRootFileProvider, IFileProvider webRooFileProvider)
+            {
+                _contentRootFileProvider = contentRootFileProvider;
+                _webRooFileProvider = webRooFileProvider;
+            }
+
+            public IFileInfo GetFileInfo(string subpath) => subpath.InvariantStartsWith(Core.Constants.SystemDirectories.AppPlugins)
+                ? _contentRootFileProvider.GetFileInfo(subpath)
+                : _webRooFileProvider.GetFileInfo(subpath);
+
+            public IDirectoryContents GetDirectoryContents(string subpath) => throw new NotSupportedException();
+
+            public IChangeToken Watch(string filter) => throw new NotSupportedException();
+        }
     }
 }
diff --git a/src/Umbraco.Web.UI.NetCore/Startup.cs b/src/Umbraco.Web.UI.NetCore/Startup.cs
index c3d3d18451..cbb8bec2da 100644
--- a/src/Umbraco.Web.UI.NetCore/Startup.cs
+++ b/src/Umbraco.Web.UI.NetCore/Startup.cs
@@ -46,7 +46,7 @@ namespace Umbraco.Web.UI.NetCore
         {
 #pragma warning disable IDE0022 // Use expression body for methods
             services.AddUmbraco(_env, _config)
-                .AddBackOffice()
+                .AddBackOffice(_env)
                 .AddWebsite()
                 .AddComposers()
                 .Build();