diff --git a/packages/frontend-dev-utils/src/createDevApp.test.tsx b/packages/frontend-dev-utils/src/createDevApp.test.tsx
index 2dc4a69101..b5beb79c1c 100644
--- a/packages/frontend-dev-utils/src/createDevApp.test.tsx
+++ b/packages/frontend-dev-utils/src/createDevApp.test.tsx
@@ -18,15 +18,25 @@ import {
   PageBlueprint,
   createFrontendPlugin,
 } from '@backstage/frontend-plugin-api';
-import { within } from '@testing-library/react';
+import { waitFor, within } from '@testing-library/react';
 import { createDevApp } from './createDevApp';
 
-const anyEnv = (process.env = { ...process.env }) as any;
+jest.setTimeout(15000);
+
+const originalEnv = process.env;
 
 describe('createDevApp', () => {
+  beforeEach(() => {
+    process.env = { ...originalEnv };
+  });
+
   afterEach(() => {
-    delete anyEnv.APP_CONFIG;
-    document.getElementById('root')?.remove();
+    document.body.innerHTML = '';
+    jest.resetAllMocks();
+  });
+
+  afterAll(() => {
+    process.env = originalEnv;
   });
 
   it('should render a dev app with a plugin', async () => {
@@ -46,7 +56,7 @@ describe('createDevApp', () => {
       ],
     });
 
-    anyEnv.APP_CONFIG = [
+    (process.env as any).APP_CONFIG = [
       {
         context: 'test',
         data: {
@@ -62,5 +72,109 @@ describe('createDevApp', () => {
 
     const body = within(document.body);
     await body.findByText('Test Plugin Page', {}, { timeout: 10000 });
-  }, 15000);
+  });
+
+  it('should forward bindRoutes to createApp', async () => {
+    jest.resetModules();
+
+    const bindRoutes = jest.fn();
+    const createApp = jest.fn(() => ({
+      createRoot: () => <div>Test App Root</div>,
+    }));
+    const render = jest.fn();
+    const createRoot = jest.fn(() => ({ render }));
+
+    jest.doMock('@backstage/frontend-defaults', () => ({
+      createApp,
+    }));
+    jest.doMock('@backstage/plugin-app', () => ({
+      __esModule: true,
+      default: {
+        withOverrides: jest.fn(() => 'app-plugin-override'),
+        getExtension: jest.fn(() => ({
+          override: jest.fn(() => 'disabled-sign-in-page'),
+        })),
+      },
+    }));
+    jest.doMock('react-dom/client', () => ({
+      __esModule: true,
+      createRoot,
+    }));
+
+    const root = document.createElement('div');
+    root.id = 'root';
+    document.body.appendChild(root);
+
+    let isolatedCreateDevApp: typeof import('./createDevApp').createDevApp;
+    jest.isolateModules(() => {
+      ({ createDevApp: isolatedCreateDevApp } = require('./createDevApp'));
+    });
+
+    isolatedCreateDevApp({
+      bindRoutes,
+      features: ['plugin-feature'] as any,
+    });
+
+    await waitFor(() => {
+      expect(createApp).toHaveBeenCalledWith({
+        bindRoutes,
+        features: ['app-plugin-override', 'plugin-feature'],
+      });
+      expect(createRoot).toHaveBeenCalledWith(root);
+    });
+  });
+
+  it('should throw a clear error when the root element is missing', () => {
+    expect(() => createDevApp({ features: [] })).toThrow(
+      "Could not find the dev app root element '#root'; make sure your dev entry HTML contains a root element with that id.",
+    );
+  });
+
+  it('should fall back to legacy react-dom rendering when createRoot is unavailable', async () => {
+    jest.resetModules();
+    delete process.env.HAS_REACT_DOM_CLIENT;
+
+    const createApp = jest.fn(() => ({
+      createRoot: () => <div>Test App Root</div>,
+    }));
+    const render = jest.fn();
+
+    jest.doMock('@backstage/frontend-defaults', () => ({
+      createApp,
+    }));
+    jest.doMock('@backstage/plugin-app', () => ({
+      __esModule: true,
+      default: {
+        withOverrides: jest.fn(() => 'app-plugin-override'),
+        getExtension: jest.fn(() => ({
+          override: jest.fn(() => 'disabled-sign-in-page'),
+        })),
+      },
+    }));
+    jest.doMock('react-dom', () => ({
+      __esModule: true,
+      render,
+    }));
+
+    const root = document.createElement('div');
+    root.id = 'root';
+    document.body.appendChild(root);
+
+    let isolatedCreateDevApp: typeof import('./createDevApp').createDevApp;
+    jest.isolateModules(() => {
+      ({ createDevApp: isolatedCreateDevApp } = require('./createDevApp'));
+    });
+
+    isolatedCreateDevApp({
+      features: ['plugin-feature'] as any,
+    });
+
+    await waitFor(() => {
+      expect(render).toHaveBeenCalled();
+      expect(createApp).toHaveBeenCalledWith({
+        bindRoutes: undefined,
+        features: ['app-plugin-override', 'plugin-feature'],
+      });
+    });
+  });
 });
diff --git a/packages/frontend-dev-utils/src/createDevApp.tsx b/packages/frontend-dev-utils/src/createDevApp.tsx
index 1f75e8d090..112901ed52 100644
--- a/packages/frontend-dev-utils/src/createDevApp.tsx
+++ b/packages/frontend-dev-utils/src/createDevApp.tsx
@@ -20,8 +20,8 @@ import {
 } from '@backstage/frontend-plugin-api';
 import { createApp, CreateAppOptions } from '@backstage/frontend-defaults';
 import appPlugin from '@backstage/plugin-app';
-import ReactDOM from 'react-dom/client';
 import { Suspense, lazy } from 'react';
+import 'react-dom';
 
 type AppPluginWithSimpleOverrides = {
   withOverrides(options: { extensions: unknown[] }): FrontendFeature;
@@ -40,6 +40,15 @@ const appPluginOverride = (
 
 const BuiCss = lazy(() => import('./BuiCss'));
 
+let ReactDOMPromise: Promise<
+  typeof import('react-dom') | typeof import('react-dom/client')
+>;
+if (process.env.HAS_REACT_DOM_CLIENT) {
+  ReactDOMPromise = import('react-dom/client');
+} else {
+  ReactDOMPromise = import('react-dom');
+}
+
 /**
  * Options for {@link createDevApp}.
  *
@@ -57,6 +66,18 @@ export interface CreateDevAppOptions {
   bindRoutes?: CreateAppOptions['bindRoutes'];
 }
 
+function getRootElement(): HTMLElement {
+  const rootElement = document.getElementById('root');
+
+  if (!rootElement) {
+    throw new Error(
+      "Could not find the dev app root element '#root'; make sure your dev entry HTML contains a root element with that id.",
+    );
+  }
+
+  return rootElement;
+}
+
 /**
  * Creates and renders a minimal development app for the new frontend system.
  *
@@ -72,6 +93,7 @@ export interface CreateDevAppOptions {
  * @public
  */
 export function createDevApp(options: CreateDevAppOptions): void {
+  const rootElement = getRootElement();
   const { features, bindRoutes } = options;
   const devFeatures: CreateAppOptions['features'] = [
     appPluginOverride,
@@ -84,10 +106,18 @@ export function createDevApp(options: CreateDevAppOptions): void {
   const app = createApp(appOptions);
   const AppRoot = app.createRoot();
 
-  ReactDOM.createRoot(document.getElementById('root')!).render(
-    <Suspense fallback={null}>
-      <BuiCss />
-      {AppRoot}
-    </Suspense>,
-  );
+  ReactDOMPromise.then(ReactDOM => {
+    const rootNode = (
+      <Suspense fallback={null}>
+        <BuiCss />
+        {AppRoot}
+      </Suspense>
+    );
+
+    if ('createRoot' in ReactDOM) {
+      ReactDOM.createRoot(rootElement).render(rootNode);
+    } else {
+      ReactDOM.render(rootNode, rootElement);
+    }
+  });
 }