diff --git a/jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/StaticHttpContentFactory.java b/jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/VirtualHttpContentFactory.java
similarity index 51%
rename from jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/StaticHttpContentFactory.java
rename to jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/VirtualHttpContentFactory.java
index 6fcfabab2f2..5ac2dda1b0a 100644
--- a/jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/StaticHttpContentFactory.java
+++ b/jetty-core/jetty-http/src/main/java/org/eclipse/jetty/http/content/VirtualHttpContentFactory.java
@@ -17,23 +17,32 @@ import java.io.IOException;
 
 import org.eclipse.jetty.util.resource.Resource;
 
-public class StaticHttpContentFactory implements HttpContent.Factory
+/**
+ * An {@link HttpContent.Factory} implementation which takes a Resource and fakes this resource as
+ * an entry in every directory. If any request is made for this resources file name, and it is not
+ * already present in that directory then the resource contained in this factory will be served instead.
+ */
+public class VirtualHttpContentFactory implements HttpContent.Factory
 {
     private final HttpContent.Factory _factory;
-    private final Resource _styleSheet;
+    private final Resource _resource;
+    private final String _contentType;
+    private final String _matchSuffix;
 
-    public StaticHttpContentFactory(HttpContent.Factory factory, Resource styleSheet)
+    public VirtualHttpContentFactory(HttpContent.Factory factory, Resource resource, String contentType)
     {
         _factory = factory;
-        _styleSheet = styleSheet;
+        _resource = resource;
+        _matchSuffix = "/" + _resource.getFileName();
+        _contentType = contentType;
     }
 
     /**
      * @return Returns the stylesheet as a Resource.
      */
-    public Resource getStyleSheet()
+    public Resource getResource()
     {
-        return _styleSheet;
+        return _resource;
     }
 
     @Override
@@ -42,10 +51,13 @@ public class StaticHttpContentFactory implements HttpContent.Factory
         HttpContent content = _factory.getContent(path);
         if (content != null)
             return content;
-
-        if ((_styleSheet != null) && (path != null) && path.endsWith("/jetty-dir.css"))
-            return new ResourceHttpContent(_styleSheet, "text/css");
-
+        if (matchResource(path))
+            return new ResourceHttpContent(_resource, _contentType);
         return null;
     }
-}
\ No newline at end of file
+
+    protected boolean matchResource(String path)
+    {
+        return (_resource != null) && (path != null) && path.endsWith(_matchSuffix);
+    }
+}
diff --git a/jetty-core/jetty-server/src/main/java/org/eclipse/jetty/server/handler/ResourceHandler.java b/jetty-core/jetty-server/src/main/java/org/eclipse/jetty/server/handler/ResourceHandler.java
index 1008773e5ff..fb81f71909a 100644
--- a/jetty-core/jetty-server/src/main/java/org/eclipse/jetty/server/handler/ResourceHandler.java
+++ b/jetty-core/jetty-server/src/main/java/org/eclipse/jetty/server/handler/ResourceHandler.java
@@ -23,8 +23,8 @@ import org.eclipse.jetty.http.content.FileMappingHttpContentFactory;
 import org.eclipse.jetty.http.content.HttpContent;
 import org.eclipse.jetty.http.content.PreCompressedHttpContentFactory;
 import org.eclipse.jetty.http.content.ResourceHttpContentFactory;
-import org.eclipse.jetty.http.content.StaticHttpContentFactory;
 import org.eclipse.jetty.http.content.ValidatingCachingHttpContentFactory;
+import org.eclipse.jetty.http.content.VirtualHttpContentFactory;
 import org.eclipse.jetty.io.ByteBufferPool;
 import org.eclipse.jetty.io.NoopByteBufferPool;
 import org.eclipse.jetty.server.Context;
@@ -106,7 +106,7 @@ public class ResourceHandler extends Handler.Wrapper
     {
         HttpContent.Factory contentFactory = new ResourceHttpContentFactory(ResourceFactory.of(getBaseResource()), getMimeTypes());
         contentFactory = new FileMappingHttpContentFactory(contentFactory);
-        contentFactory = new StaticHttpContentFactory(contentFactory, getStyleSheet());
+        contentFactory = new VirtualHttpContentFactory(contentFactory, getStyleSheet(), "text/css");
         contentFactory = new PreCompressedHttpContentFactory(contentFactory, getPrecompressedFormats());
         contentFactory = new ValidatingCachingHttpContentFactory(contentFactory, Duration.ofSeconds(1).toMillis(), getByteBufferPool());
         return contentFactory;
diff --git a/jetty-core/jetty-server/src/test/java/org/eclipse/jetty/server/handler/ResourceHandlerTest.java b/jetty-core/jetty-server/src/test/java/org/eclipse/jetty/server/handler/ResourceHandlerTest.java
index 41c5e720ea0..13807825810 100644
--- a/jetty-core/jetty-server/src/test/java/org/eclipse/jetty/server/handler/ResourceHandlerTest.java
+++ b/jetty-core/jetty-server/src/test/java/org/eclipse/jetty/server/handler/ResourceHandlerTest.java
@@ -47,8 +47,8 @@ import org.eclipse.jetty.http.content.FileMappingHttpContentFactory;
 import org.eclipse.jetty.http.content.HttpContent;
 import org.eclipse.jetty.http.content.PreCompressedHttpContentFactory;
 import org.eclipse.jetty.http.content.ResourceHttpContentFactory;
-import org.eclipse.jetty.http.content.StaticHttpContentFactory;
 import org.eclipse.jetty.http.content.ValidatingCachingHttpContentFactory;
+import org.eclipse.jetty.http.content.VirtualHttpContentFactory;
 import org.eclipse.jetty.logging.StacklessLogging;
 import org.eclipse.jetty.server.Handler;
 import org.eclipse.jetty.server.HttpConfiguration;
@@ -668,7 +668,7 @@ public class ResourceHandlerTest
             {
                 HttpContent.Factory contentFactory = new ResourceHttpContentFactory(ResourceFactory.of(getBaseResource()), getMimeTypes());
                 contentFactory = new FileMappingHttpContentFactory(contentFactory);
-                contentFactory = new StaticHttpContentFactory(contentFactory, getStyleSheet());
+                contentFactory = new VirtualHttpContentFactory(contentFactory, getStyleSheet(), "text/css");
                 contentFactory = new PreCompressedHttpContentFactory(contentFactory, getPrecompressedFormats());
                 contentFactory = new ValidatingCachingHttpContentFactory(contentFactory, 0, getByteBufferPool());
                 return contentFactory;
diff --git a/jetty-ee10/jetty-ee10-servlet/src/main/java/org/eclipse/jetty/ee10/servlet/DefaultServlet.java b/jetty-ee10/jetty-ee10-servlet/src/main/java/org/eclipse/jetty/ee10/servlet/DefaultServlet.java
index f0ab2a2e588..a7671c6eefe 100644
--- a/jetty-ee10/jetty-ee10-servlet/src/main/java/org/eclipse/jetty/ee10/servlet/DefaultServlet.java
+++ b/jetty-ee10/jetty-ee10-servlet/src/main/java/org/eclipse/jetty/ee10/servlet/DefaultServlet.java
@@ -57,8 +57,8 @@ import org.eclipse.jetty.http.content.FileMappingHttpContentFactory;
 import org.eclipse.jetty.http.content.HttpContent;
 import org.eclipse.jetty.http.content.PreCompressedHttpContentFactory;
 import org.eclipse.jetty.http.content.ResourceHttpContentFactory;
-import org.eclipse.jetty.http.content.StaticHttpContentFactory;
 import org.eclipse.jetty.http.content.ValidatingCachingHttpContentFactory;
+import org.eclipse.jetty.http.content.VirtualHttpContentFactory;
 import org.eclipse.jetty.io.ByteBufferInputStream;
 import org.eclipse.jetty.io.ByteBufferPool;
 import org.eclipse.jetty.io.NoopByteBufferPool;
@@ -158,7 +158,7 @@ public class DefaultServlet extends HttpServlet
             if (getInitBoolean("useFileMappedBuffer", false))
                 contentFactory = new FileMappingHttpContentFactory(contentFactory);
 
-            contentFactory = new StaticHttpContentFactory(contentFactory, styleSheet);
+            contentFactory = new VirtualHttpContentFactory(contentFactory, styleSheet, "text/css");
             contentFactory = new PreCompressedHttpContentFactory(contentFactory, precompressedFormats);
 
             int maxCacheSize = getInitInt("maxCacheSize", -2);
diff --git a/jetty-ee9/jetty-ee9-nested/src/main/java/org/eclipse/jetty/ee9/nested/ResourceHandler.java b/jetty-ee9/jetty-ee9-nested/src/main/java/org/eclipse/jetty/ee9/nested/ResourceHandler.java
index fbd3db81347..9383ee2adb6 100644
--- a/jetty-ee9/jetty-ee9-nested/src/main/java/org/eclipse/jetty/ee9/nested/ResourceHandler.java
+++ b/jetty-ee9/jetty-ee9-nested/src/main/java/org/eclipse/jetty/ee9/nested/ResourceHandler.java
@@ -33,8 +33,8 @@ import org.eclipse.jetty.http.content.FileMappingHttpContentFactory;
 import org.eclipse.jetty.http.content.HttpContent;
 import org.eclipse.jetty.http.content.PreCompressedHttpContentFactory;
 import org.eclipse.jetty.http.content.ResourceHttpContentFactory;
-import org.eclipse.jetty.http.content.StaticHttpContentFactory;
 import org.eclipse.jetty.http.content.ValidatingCachingHttpContentFactory;
+import org.eclipse.jetty.http.content.VirtualHttpContentFactory;
 import org.eclipse.jetty.io.ByteBufferPool;
 import org.eclipse.jetty.io.NoopByteBufferPool;
 import org.eclipse.jetty.server.Server;
@@ -134,7 +134,7 @@ public class ResourceHandler extends HandlerWrapper implements ResourceFactory,
     {
         HttpContent.Factory contentFactory = new ResourceHttpContentFactory(this, _mimeTypes);
         contentFactory = new FileMappingHttpContentFactory(contentFactory);
-        contentFactory = new StaticHttpContentFactory(contentFactory, getStyleSheet());
+        contentFactory = new VirtualHttpContentFactory(contentFactory, getStyleSheet(), "text/css");
         contentFactory = new PreCompressedHttpContentFactory(contentFactory, _resourceService.getPrecompressedFormats());
         contentFactory = new ValidatingCachingHttpContentFactory(contentFactory, Duration.ofSeconds(1).toMillis(), _byteBufferPool);
         return contentFactory;
diff --git a/jetty-ee9/jetty-ee9-servlet/src/main/java/org/eclipse/jetty/ee9/servlet/DefaultServlet.java b/jetty-ee9/jetty-ee9-servlet/src/main/java/org/eclipse/jetty/ee9/servlet/DefaultServlet.java
index 6bec020b258..e88832fde11 100644
--- a/jetty-ee9/jetty-ee9-servlet/src/main/java/org/eclipse/jetty/ee9/servlet/DefaultServlet.java
+++ b/jetty-ee9/jetty-ee9-servlet/src/main/java/org/eclipse/jetty/ee9/servlet/DefaultServlet.java
@@ -39,8 +39,8 @@ import org.eclipse.jetty.http.content.FileMappingHttpContentFactory;
 import org.eclipse.jetty.http.content.HttpContent;
 import org.eclipse.jetty.http.content.PreCompressedHttpContentFactory;
 import org.eclipse.jetty.http.content.ResourceHttpContentFactory;
-import org.eclipse.jetty.http.content.StaticHttpContentFactory;
 import org.eclipse.jetty.http.content.ValidatingCachingHttpContentFactory;
+import org.eclipse.jetty.http.content.VirtualHttpContentFactory;
 import org.eclipse.jetty.io.ByteBufferPool;
 import org.eclipse.jetty.io.NoopByteBufferPool;
 import org.eclipse.jetty.server.Server;
@@ -253,7 +253,7 @@ public class DefaultServlet extends HttpServlet implements ResourceFactory, Welc
             contentFactory = new ResourceHttpContentFactory(this, _mimeTypes);
             if (_useFileMappedBuffer)
                 contentFactory = new FileMappingHttpContentFactory(contentFactory);
-            contentFactory = new StaticHttpContentFactory(contentFactory, _styleSheet);
+            contentFactory = new VirtualHttpContentFactory(contentFactory, _styleSheet, "text/css");
             contentFactory = new PreCompressedHttpContentFactory(contentFactory, _resourceService.getPrecompressedFormats());
 
             int maxCacheSize = getInitInt("maxCacheSize", -2);