diff --git a/.changeset/thin-experts-sing.md b/.changeset/thin-experts-sing.md
new file mode 100644
index 0000000000..55aa8eac90
--- /dev/null
+++ b/.changeset/thin-experts-sing.md
@@ -0,0 +1,10 @@
+---
+'@backstage/core-compat-api': patch
+---
+
+The `convertLegacyApp` has received the following changes:
+
+- `null` routes will now be ignored.
+- Converted routes no longer need to belong to a plugin, falling back to a `converted-orphan-routes` plugin instead.
+- The generate layout override extension is now properly attached to the `app/root` extension.
+- Converted root elements are now automatically wrapped with `compatWrapper`.
diff --git a/packages/core-compat-api/src/collectLegacyRoutes.test.tsx b/packages/core-compat-api/src/collectLegacyRoutes.test.tsx
index a28bda6dea..ce0b055c00 100644
--- a/packages/core-compat-api/src/collectLegacyRoutes.test.tsx
+++ b/packages/core-compat-api/src/collectLegacyRoutes.test.tsx
@@ -48,8 +48,10 @@ describe('collectLegacyRoutes', () => {
       <FlatRoutes>
         <Route path="/score-board" element={<ScoreBoardPage />} />
         <Route path="/stackstorm" element={<StackstormPage />} />
+        <Route path="/other" element={<div />} />
         <Route path="/puppetdb" element={<PuppetDbPage />} />
         <Route path="/puppetdb" element={<PuppetDbPage />} />
+        <Route path="/other" element={<div />} />
       </FlatRoutes>,
     );
 
@@ -96,6 +98,23 @@ describe('collectLegacyRoutes', () => {
           },
         ],
       },
+      {
+        id: 'converted-orphan-routes',
+        extensions: [
+          {
+            id: 'page:converted-orphan-routes',
+            attachTo: { id: 'app/routes', input: 'routes' },
+            disabled: false,
+            defaultConfig: {},
+          },
+          {
+            id: 'page:converted-orphan-routes/2',
+            attachTo: { id: 'app/routes', input: 'routes' },
+            disabled: false,
+            defaultConfig: {},
+          },
+        ],
+      },
       {
         id: 'puppetDb',
         extensions: [
@@ -378,8 +397,6 @@ describe('collectLegacyRoutes', () => {
           <Route element={<Navigate to="/somewhere" />} />
         </FlatRoutes>,
       ),
-    ).toThrow(
-      /Route with path undefined has en element that can not be converted/,
-    );
+    ).toThrow(/Route element inside FlatRoutes had no path prop value given/);
   });
 });
diff --git a/packages/core-compat-api/src/collectLegacyRoutes.tsx b/packages/core-compat-api/src/collectLegacyRoutes.tsx
index f3d94dc4b9..b0a55f9ddd 100644
--- a/packages/core-compat-api/src/collectLegacyRoutes.tsx
+++ b/packages/core-compat-api/src/collectLegacyRoutes.tsx
@@ -18,6 +18,7 @@ import {
   AnyRouteRefParams,
   BackstagePlugin as LegacyBackstagePlugin,
   RouteRef,
+  createPlugin,
   getComponentData,
 } from '@backstage/core-plugin-api';
 import {
@@ -167,6 +168,9 @@ export function collectLegacyRoutes(
     return () => String(currentIndex++);
   })();
 
+  // Placeholder plugin for any routes that don't belong to a plugin
+  const orphanRoutesPlugin = createPlugin({ id: 'converted-orphan-routes' });
+
   const getPluginExtensions = (plugin: LegacyBackstagePlugin) => {
     let extensions = pluginExtensions.get(plugin);
     if (!extensions) {
@@ -179,6 +183,9 @@ export function collectLegacyRoutes(
   React.Children.forEach(
     flatRoutesElement.props.children,
     (route: ReactNode) => {
+      if (route === null) {
+        return;
+      }
       // TODO(freben): Handle feature flag and permissions framework wrapper elements
       if (!React.isValidElement(route)) {
         throw new Error(
@@ -192,20 +199,13 @@ export function collectLegacyRoutes(
       }
       const routeElement = route.props.element;
       const path: string | undefined = route.props.path;
-      const plugin = getComponentData<LegacyBackstagePlugin>(
-        routeElement,
-        'core.plugin',
-      );
+      const plugin =
+        getComponentData<LegacyBackstagePlugin>(routeElement, 'core.plugin') ??
+        orphanRoutesPlugin;
       const routeRef = getComponentData<RouteRef>(
         routeElement,
         'core.mountPoint',
       );
-      if (!plugin) {
-        throw new Error(
-          // TODO(vinzscam): add See <link-to-app-migration-docs> for more info
-          `Route with path ${path} has en element that can not be converted as it does not belong to a plugin. Make sure that the top-level React element of the element prop is an extension from a Backstage plugin, or remove the Route completely.`,
-        );
-      }
       if (path === undefined) {
         throw new Error(
           `Route element inside FlatRoutes had no path prop value given`,
diff --git a/packages/core-compat-api/src/convertLegacyApp.test.tsx b/packages/core-compat-api/src/convertLegacyApp.test.tsx
index 224ab46221..7153fcb4be 100644
--- a/packages/core-compat-api/src/convertLegacyApp.test.tsx
+++ b/packages/core-compat-api/src/convertLegacyApp.test.tsx
@@ -114,7 +114,7 @@ describe('convertLegacyApp', () => {
         extensions: [
           {
             id: 'app/layout',
-            attachTo: { id: 'app', input: 'root' },
+            attachTo: { id: 'app/root', input: 'children' },
             disabled: false,
           },
           {
diff --git a/packages/core-compat-api/src/convertLegacyApp.ts b/packages/core-compat-api/src/convertLegacyApp.ts
index 3f35c78408..f098d090ed 100644
--- a/packages/core-compat-api/src/convertLegacyApp.ts
+++ b/packages/core-compat-api/src/convertLegacyApp.ts
@@ -32,6 +32,7 @@ import {
 } from '@backstage/frontend-plugin-api';
 import { getComponentData } from '@backstage/core-plugin-api';
 import { collectLegacyRoutes } from './collectLegacyRoutes';
+import { compatWrapper } from './compatWrapper';
 
 function selectChildren(
   rootNode: ReactNode,
@@ -106,7 +107,7 @@ export function convertLegacyApp(
 
   const CoreLayoutOverride = createExtension({
     name: 'layout',
-    attachTo: { id: 'app', input: 'root' },
+    attachTo: { id: 'app/root', input: 'children' },
     inputs: {
       content: createExtensionInput([coreExtensionData.reactElement], {
         singleton: true,
@@ -117,10 +118,12 @@ export function convertLegacyApp(
       // Clone the root element, this replaces the FlatRoutes declared in the app with out content input
       return [
         coreExtensionData.reactElement(
-          React.cloneElement(
-            rootEl,
-            undefined,
-            inputs.content.get(coreExtensionData.reactElement),
+          compatWrapper(
+            React.cloneElement(
+              rootEl,
+              undefined,
+              inputs.content.get(coreExtensionData.reactElement),
+            ),
           ),
         ),
       ];