diff --git a/.changeset/brave-eels-allow.md b/.changeset/brave-eels-allow.md
new file mode 100644
index 0000000000..8fbe7ba8d2
--- /dev/null
+++ b/.changeset/brave-eels-allow.md
@@ -0,0 +1,5 @@
+---
+'@backstage/core-app-api': minor
+---
+
+Updated the React Router wiring to make use of the new `basename` property of the router components in React Router v6 stable. To implement this, a new optional `basename` property has been added to the `Router` app component, which can be forwarded to the concrete router implementation in order to support this new behavior. This is done by default in any app that does not have a `Router` component override.
diff --git a/packages/core-app-api/src/app/AppManager.compat.test.tsx b/packages/core-app-api/src/app/AppManager.compat.test.tsx
new file mode 100644
index 0000000000..bdebd79dc4
--- /dev/null
+++ b/packages/core-app-api/src/app/AppManager.compat.test.tsx
@@ -0,0 +1,107 @@
+/*
+ * Copyright 2020 The Backstage Authors
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+import tlr, { render } from '@testing-library/react';
+import React from 'react';
+
+describe.each(['beta', 'stable'])('react-router %s', rrVersion => {
+  beforeAll(() => {
+    jest.doMock('react', () => React);
+    // This has some side effects, so need this to be stable to avoid re-require
+    jest.doMock('@testing-library/react', () => tlr);
+    jest.doMock('react-router', () =>
+      rrVersion === 'beta'
+        ? jest.requireActual('react-router-beta')
+        : jest.requireActual('react-router-stable'),
+    );
+    jest.doMock('react-router-dom', () =>
+      rrVersion === 'beta'
+        ? jest.requireActual('react-router-dom-beta')
+        : jest.requireActual('react-router-dom-stable'),
+    );
+  });
+
+  afterAll(() => {
+    jest.resetModules();
+  });
+
+  function requireDeps() {
+    return {
+      ...(require('./AppManager') as typeof import('./AppManager')),
+      ...(require('../routing') as typeof import('../routing')),
+      ...(require('react-router-dom') as typeof import('react-router-dom')),
+      ...(require('@backstage/test-utils') as typeof import('@backstage/test-utils')),
+    };
+  }
+
+  describe('AppManager', () => {
+    it('supports base path', async () => {
+      const { AppManager, MemoryRouter, Navigate, Route, FlatRoutes } =
+        requireDeps();
+      const app = new AppManager({
+        apis: [],
+        defaultApis: [],
+        themes: [
+          {
+            id: 'light',
+            title: 'Light Theme',
+            variant: 'light',
+            Provider: ({ children }) => <>{children}</>,
+          },
+        ],
+        icons: {} as any,
+        plugins: [],
+        components: {
+          NotFoundErrorPage: () => null,
+          BootErrorPage: () => null,
+          Progress: () => null,
+          Router: ({ children, basename }) => (
+            <MemoryRouter
+              initialEntries={['/foo']}
+              basename={basename}
+              children={children}
+            />
+          ),
+          ErrorBoundaryFallback: () => null,
+          ThemeProvider: ({ children }) => <>{children}</>,
+        },
+        configLoader: async () => [
+          {
+            context: 'test',
+            data: { app: { baseUrl: 'http://localhost/foo' } },
+          },
+        ],
+        bindRoutes: () => {},
+      });
+
+      const AppProvider = app.getProvider();
+      const AppRouter = app.getRouter();
+
+      const rendered = render(
+        <AppProvider>
+          <AppRouter>
+            <FlatRoutes>
+              <Route path="/" element={<Navigate to="bar" />} />
+              <Route path="/bar" element={<span>bar</span>} />
+            </FlatRoutes>
+          </AppRouter>
+        </AppProvider>,
+      );
+
+      await expect(rendered.findByText('bar')).resolves.toBeInTheDocument();
+    });
+  });
+});
diff --git a/packages/core-app-api/src/app/AppManager.stable.test.tsx b/packages/core-app-api/src/app/AppManager.stable.test.tsx
new file mode 100644
index 0000000000..a9948a6070
--- /dev/null
+++ b/packages/core-app-api/src/app/AppManager.stable.test.tsx
@@ -0,0 +1,118 @@
+/*
+ * Copyright 2020 The Backstage Authors
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+import { render } from '@testing-library/react';
+import React from 'react';
+import { MemoryRouter, Navigate, Route } from 'react-router-dom';
+import { FlatRoutes } from '../routing';
+import { AppManager } from './AppManager';
+import { AppOptions } from './types';
+
+jest.mock('react-router', () => jest.requireActual('react-router-stable'));
+jest.mock('react-router-dom', () =>
+  jest.requireActual('react-router-dom-stable'),
+);
+
+const mockAppOptions: AppOptions = {
+  apis: [],
+  defaultApis: [],
+  themes: [
+    {
+      id: 'light',
+      title: 'Light Theme',
+      variant: 'light',
+      Provider: ({ children }) => <>{children}</>,
+    },
+  ],
+  icons: {} as any,
+  plugins: [],
+  components: {
+    NotFoundErrorPage: () => null,
+    BootErrorPage: () => null,
+    Progress: () => null,
+    Router: props => <MemoryRouter {...props} />,
+    ErrorBoundaryFallback: () => null,
+    ThemeProvider: ({ children }) => <>{children}</>,
+  },
+  configLoader: async () => [],
+  bindRoutes: () => {},
+};
+
+describe('AppManager', () => {
+  it('supports base path', async () => {
+    const app = new AppManager({
+      ...mockAppOptions,
+      components: {
+        ...mockAppOptions.components,
+        Router: props => <MemoryRouter {...props} initialEntries={['/foo']} />,
+      },
+      configLoader: async () => [
+        {
+          context: 'test',
+          data: { app: { baseUrl: 'http://localhost/foo' } },
+        },
+      ],
+    });
+
+    const AppProvider = app.getProvider();
+    const AppRouter = app.getRouter();
+
+    const rendered = render(
+      <AppProvider>
+        <AppRouter>
+          <FlatRoutes>
+            <Route path="/" element={<Navigate to="bar" />} />
+            <Route path="/bar" element={<span>bar</span>} />
+          </FlatRoutes>
+        </AppRouter>
+      </AppProvider>,
+    );
+
+    await expect(rendered.findByText('bar')).resolves.toBeInTheDocument();
+  });
+
+  it('supports base path with absolute navigation', async () => {
+    const app = new AppManager({
+      ...mockAppOptions,
+      components: {
+        ...mockAppOptions.components,
+        Router: props => <MemoryRouter {...props} initialEntries={['/foo']} />,
+      },
+      configLoader: async () => [
+        {
+          context: 'test',
+          data: { app: { baseUrl: 'http://localhost/foo' } },
+        },
+      ],
+    });
+
+    const AppProvider = app.getProvider();
+    const AppRouter = app.getRouter();
+
+    const rendered = render(
+      <AppProvider>
+        <AppRouter>
+          <FlatRoutes>
+            <Route path="/" element={<Navigate to="/bar" />} />
+            <Route path="/bar" element={<span>bar</span>} />
+          </FlatRoutes>
+        </AppRouter>
+      </AppProvider>,
+    );
+
+    await expect(rendered.findByText('bar')).resolves.toBeInTheDocument();
+  });
+});
diff --git a/packages/core-app-api/src/app/AppManager.tsx b/packages/core-app-api/src/app/AppManager.tsx
index 89402476e3..0ca09c0a0c 100644
--- a/packages/core-app-api/src/app/AppManager.tsx
+++ b/packages/core-app-api/src/app/AppManager.tsx
@@ -99,6 +99,21 @@ const InternalAppContext = createContext<{
  * The returned path does not have a trailing slash.
  */
 function getBasePath(configApi: Config) {
+  if (!isReactRouterBeta()) {
+    // When using rr v6 stable the base path is handled through the
+    // basename prop on the router component instead.
+    return '';
+  }
+
+  return readBasePath(configApi);
+}
+
+/**
+ * Read the configured base path.
+ *
+ * The returned path does not have a trailing slash.
+ */
+function readBasePath(configApi: ConfigApi) {
   let { pathname } = new URL(
     configApi.getOptionalString('app.baseUrl') ?? '/',
     'http://dummy.dev', // baseUrl can be specified as just a path
@@ -361,7 +376,7 @@ export class AppManager implements BackstageApp {
 
     const AppRouter = ({ children }: PropsWithChildren<{}>) => {
       const configApi = useApi(configApiRef);
-      const basePath = getBasePath(configApi);
+      const basePath = readBasePath(configApi);
       const mountPath = `${basePath}/*`;
       const { routeObjects } = useContext(InternalAppContext);
 
@@ -390,23 +405,43 @@ export class AppManager implements BackstageApp {
           { signOutTargetUrl: basePath || '/' },
         );
 
+        if (isReactRouterBeta()) {
+          return (
+            <RouterComponent>
+              <RouteTracker routeObjects={routeObjects} />
+              <Routes>
+                <Route path={mountPath} element={<>{children}</>} />
+              </Routes>
+            </RouterComponent>
+          );
+        }
+
+        return (
+          <RouterComponent basename={basePath}>
+            <RouteTracker routeObjects={routeObjects} />
+            {children}
+          </RouterComponent>
+        );
+      }
+
+      if (isReactRouterBeta()) {
         return (
           <RouterComponent>
             <RouteTracker routeObjects={routeObjects} />
-            <Routes>
-              <Route path={mountPath} element={<>{children}</>} />
-            </Routes>
+            <SignInPageWrapper component={SignInPageComponent}>
+              <Routes>
+                <Route path={mountPath} element={<>{children}</>} />
+              </Routes>
+            </SignInPageWrapper>
           </RouterComponent>
         );
       }
 
       return (
-        <RouterComponent>
+        <RouterComponent basename={basePath}>
           <RouteTracker routeObjects={routeObjects} />
           <SignInPageWrapper component={SignInPageComponent}>
-            <Routes>
-              <Route path={mountPath} element={<>{children}</>} />
-            </Routes>
+            <>{children}</>
           </SignInPageWrapper>
         </RouterComponent>
       );
diff --git a/packages/core-app-api/src/app/types.ts b/packages/core-app-api/src/app/types.ts
index 39bf9c0554..70022534a1 100644
--- a/packages/core-app-api/src/app/types.ts
+++ b/packages/core-app-api/src/app/types.ts
@@ -69,7 +69,7 @@ export type AppComponents = {
   NotFoundErrorPage: ComponentType<{}>;
   BootErrorPage: ComponentType<BootErrorPageProps>;
   Progress: ComponentType<{}>;
-  Router: ComponentType<{}>;
+  Router: ComponentType<{ basename?: string }>;
   ErrorBoundaryFallback: ComponentType<ErrorBoundaryFallbackProps>;
   ThemeProvider?: ComponentType<{}>;