diff --git a/.changeset/fair-ants-work.md b/.changeset/fair-ants-work.md
new file mode 100644
index 0000000000..4cf3c80488
--- /dev/null
+++ b/.changeset/fair-ants-work.md
@@ -0,0 +1,7 @@
+---
+'@backstage/backend-app-api': minor
+---
+
+**BREAKING**: The `httpRouterFactory` now accepts a `getPath` option rather than `indexPlugin`. To set up custom index path, configure the new `rootHttpRouterFactory` with a custom `indexPath` instead.
+
+Added an implementation for the new `rootHttpRouterServiceRef`.
diff --git a/.changeset/gorgeous-days-applaud.md b/.changeset/gorgeous-days-applaud.md
new file mode 100644
index 0000000000..a34307d720
--- /dev/null
+++ b/.changeset/gorgeous-days-applaud.md
@@ -0,0 +1,5 @@
+---
+'@backstage/backend-plugin-api': patch
+---
+
+Added a new `rootHttpRouterServiceRef` and `RootHttpRouterService` interface.
diff --git a/.changeset/little-beans-hammer.md b/.changeset/little-beans-hammer.md
new file mode 100644
index 0000000000..d998f5f5ba
--- /dev/null
+++ b/.changeset/little-beans-hammer.md
@@ -0,0 +1,5 @@
+---
+'@backstage/backend-test-utils': patch
+---
+
+The `startTestBackend` setup now includes default implementations for all core services.
diff --git a/.changeset/tiny-cooks-hide.md b/.changeset/tiny-cooks-hide.md
new file mode 100644
index 0000000000..feab4b65d2
--- /dev/null
+++ b/.changeset/tiny-cooks-hide.md
@@ -0,0 +1,5 @@
+---
+'@backstage/backend-defaults': patch
+---
+
+The new root HTTP router service is now installed by default.
diff --git a/packages/backend-app-api/api-report.md b/packages/backend-app-api/api-report.md
index fa3f3bec2e..dcf3ced5e8 100644
--- a/packages/backend-app-api/api-report.md
+++ b/packages/backend-app-api/api-report.md
@@ -8,11 +8,13 @@ import { CacheService } from '@backstage/backend-plugin-api';
 import { ConfigService } from '@backstage/backend-plugin-api';
 import { DatabaseService } from '@backstage/backend-plugin-api';
 import { ExtensionPoint } from '@backstage/backend-plugin-api';
+import { Handler } from 'express';
 import { HttpRouterService } from '@backstage/backend-plugin-api';
 import { LifecycleService } from '@backstage/backend-plugin-api';
 import { LoggerService } from '@backstage/backend-plugin-api';
 import { PermissionsService } from '@backstage/backend-plugin-api';
 import { PluginEndpointDiscovery } from '@backstage/backend-common';
+import { RootHttpRouterService } from '@backstage/backend-plugin-api';
 import { RootLifecycleService } from '@backstage/backend-plugin-api';
 import { RootLoggerService } from '@backstage/backend-plugin-api';
 import { SchedulerService } from '@backstage/backend-plugin-api';
@@ -69,7 +71,7 @@ export const httpRouterFactory: (
 
 // @public (undocumented)
 export type HttpRouterFactoryOptions = {
-  indexPlugin?: string;
+  getPath(pluginId: string): string;
 };
 
 // @public
@@ -87,6 +89,17 @@ export const permissionsFactory: (
   options?: undefined,
 ) => ServiceFactory<PermissionsService>;
 
+// @public (undocumented)
+export const rootHttpRouterFactory: (
+  options?: RootHttpRouterFactoryOptions | undefined,
+) => ServiceFactory<RootHttpRouterService>;
+
+// @public (undocumented)
+export type RootHttpRouterFactoryOptions = {
+  indexPath?: string | false;
+  middleware?: Handler[];
+};
+
 // @public
 export const rootLifecycleFactory: (
   options?: undefined,
diff --git a/packages/backend-app-api/package.json b/packages/backend-app-api/package.json
index 93230341df..80598ec93d 100644
--- a/packages/backend-app-api/package.json
+++ b/packages/backend-app-api/package.json
@@ -38,6 +38,7 @@
     "@backstage/backend-tasks": "workspace:^",
     "@backstage/errors": "workspace:^",
     "@backstage/plugin-permission-node": "workspace:^",
+    "@types/express": "^4.17.6",
     "express": "^4.17.1",
     "express-promise-router": "^4.1.0",
     "winston": "^3.2.1"
diff --git a/packages/backend-app-api/src/services/implementations/httpRouterService.test.ts b/packages/backend-app-api/src/services/implementations/httpRouterService.test.ts
new file mode 100644
index 0000000000..89f6db2ac8
--- /dev/null
+++ b/packages/backend-app-api/src/services/implementations/httpRouterService.test.ts
@@ -0,0 +1,70 @@
+/*
+ * Copyright 2022 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 {
+  HttpRouterService,
+  ServiceFactory,
+} from '@backstage/backend-plugin-api';
+import { httpRouterFactory } from './httpRouterService';
+
+describe('httpRouterFactory', () => {
+  it('should register plugin paths', async () => {
+    const rootHttpRouter = { use: jest.fn() };
+    const factory = httpRouterFactory() as Exclude<
+      ServiceFactory<HttpRouterService>,
+      { scope: 'root' }
+    >;
+    const innerFactory = await factory.factory({ rootHttpRouter });
+
+    const handler1 = () => {};
+    const router1 = await innerFactory({ plugin: { getId: () => 'test1' } });
+    router1.use(handler1);
+    expect(rootHttpRouter.use).toHaveBeenCalledTimes(1);
+    expect(rootHttpRouter.use).toHaveBeenCalledWith('/api/test1', handler1);
+
+    const handler2 = () => {};
+    const router2 = await innerFactory({ plugin: { getId: () => 'test2' } });
+    router2.use(handler2);
+    expect(rootHttpRouter.use).toHaveBeenCalledTimes(2);
+    expect(rootHttpRouter.use).toHaveBeenCalledWith('/api/test2', handler2);
+  });
+
+  it('should use custom path generator', async () => {
+    const rootHttpRouter = { use: jest.fn() };
+    const factory = httpRouterFactory({
+      getPath: id => `/some/${id}/path`,
+    }) as Exclude<ServiceFactory<HttpRouterService>, { scope: 'root' }>;
+    const innerFactory = await factory.factory({ rootHttpRouter });
+
+    const handler1 = () => {};
+    const router1 = await innerFactory({ plugin: { getId: () => 'test1' } });
+    router1.use(handler1);
+    expect(rootHttpRouter.use).toHaveBeenCalledTimes(1);
+    expect(rootHttpRouter.use).toHaveBeenCalledWith(
+      '/some/test1/path',
+      handler1,
+    );
+
+    const handler2 = () => {};
+    const router2 = await innerFactory({ plugin: { getId: () => 'test2' } });
+    router2.use(handler2);
+    expect(rootHttpRouter.use).toHaveBeenCalledTimes(2);
+    expect(rootHttpRouter.use).toHaveBeenCalledWith(
+      '/some/test2/path',
+      handler2,
+    );
+  });
+});
diff --git a/packages/backend-app-api/src/services/implementations/httpRouterService.ts b/packages/backend-app-api/src/services/implementations/httpRouterService.ts
index 2021589a50..f1fc089ea3 100644
--- a/packages/backend-app-api/src/services/implementations/httpRouterService.ts
+++ b/packages/backend-app-api/src/services/implementations/httpRouterService.ts
@@ -18,49 +18,33 @@ import {
   createServiceFactory,
   coreServices,
 } from '@backstage/backend-plugin-api';
-import Router from 'express-promise-router';
 import { Handler } from 'express';
-import { createServiceBuilder } from '@backstage/backend-common';
 
 /**
  * @public
  */
 export type HttpRouterFactoryOptions = {
   /**
-   * The plugin ID used for the index route. Defaults to 'app'
+   * A callback used to generate the path for each plugin, defaults to `/api/{pluginId}`.
    */
-  indexPlugin?: string;
+  getPath(pluginId: string): string;
 };
 
 /** @public */
 export const httpRouterFactory = createServiceFactory({
   service: coreServices.httpRouter,
   deps: {
-    config: coreServices.config,
     plugin: coreServices.pluginMetadata,
+    rootHttpRouter: coreServices.rootHttpRouter,
   },
-  async factory({ config }, options?: HttpRouterFactoryOptions) {
-    const defaultPluginId = options?.indexPlugin ?? 'app';
-
-    const apiRouter = Router();
-    const rootRouter = Router();
-
-    const service = createServiceBuilder(module)
-      .loadConfig(config)
-      .addRouter('/api', apiRouter)
-      .addRouter('', rootRouter);
-
-    await service.start();
+  async factory({ rootHttpRouter }, options?: HttpRouterFactoryOptions) {
+    const getPath = options?.getPath ?? (id => `/api/${id}`);
 
     return async ({ plugin }) => {
-      const pluginId = plugin.getId();
+      const path = getPath(plugin.getId());
       return {
         use(handler: Handler) {
-          if (pluginId === defaultPluginId) {
-            rootRouter.use(handler);
-          } else {
-            apiRouter.use(`/${pluginId}`, handler);
-          }
+          rootHttpRouter.use(path, handler);
         },
       };
     };
diff --git a/packages/backend-app-api/src/services/implementations/index.ts b/packages/backend-app-api/src/services/implementations/index.ts
index c87011d570..2365ff36f4 100644
--- a/packages/backend-app-api/src/services/implementations/index.ts
+++ b/packages/backend-app-api/src/services/implementations/index.ts
@@ -25,6 +25,8 @@ export { schedulerFactory } from './schedulerService';
 export { tokenManagerFactory } from './tokenManagerService';
 export { urlReaderFactory } from './urlReaderService';
 export { httpRouterFactory } from './httpRouterService';
+export { rootHttpRouterFactory } from './rootHttpRouterService';
 export { lifecycleFactory } from './lifecycleService';
 export { rootLifecycleFactory } from './rootLifecycleService';
 export type { HttpRouterFactoryOptions } from './httpRouterService';
+export type { RootHttpRouterFactoryOptions } from './rootHttpRouterService';
diff --git a/packages/backend-app-api/src/services/implementations/rootHttpRouterService.test.ts b/packages/backend-app-api/src/services/implementations/rootHttpRouterService.test.ts
new file mode 100644
index 0000000000..fea99b0df9
--- /dev/null
+++ b/packages/backend-app-api/src/services/implementations/rootHttpRouterService.test.ts
@@ -0,0 +1,31 @@
+/*
+ * Copyright 2022 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 { findConflictingPath } from './rootHttpRouterService';
+
+describe('findConflictingPath', () => {
+  it('finds conflicts when present', () => {
+    expect(findConflictingPath(['/a'], '/a')).toBe('/a');
+    expect(findConflictingPath(['/b'], '/a')).toBe(undefined);
+    expect(findConflictingPath(['/a'], '/a/b')).toBe('/a');
+    expect(findConflictingPath(['/a'], '/aa/b')).toBe(undefined);
+    expect(findConflictingPath(['/aa'], '/a/b')).toBe(undefined);
+    expect(findConflictingPath(['/a/b'], '/a')).toBe('/a/b');
+    expect(findConflictingPath(['/a/b'], '/aa')).toBe(undefined);
+    expect(findConflictingPath(['/b/a'], '/a')).toBe(undefined);
+    expect(findConflictingPath(['/a'], '/aa')).toBe(undefined);
+  });
+});
diff --git a/packages/backend-app-api/src/services/implementations/rootHttpRouterService.ts b/packages/backend-app-api/src/services/implementations/rootHttpRouterService.ts
new file mode 100644
index 0000000000..dae7474793
--- /dev/null
+++ b/packages/backend-app-api/src/services/implementations/rootHttpRouterService.ts
@@ -0,0 +1,125 @@
+/*
+ * Copyright 2022 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 {
+  createServiceFactory,
+  coreServices,
+} from '@backstage/backend-plugin-api';
+import Router from 'express-promise-router';
+import { Handler } from 'express';
+import { createServiceBuilder } from '@backstage/backend-common';
+
+/**
+ * @public
+ */
+export type RootHttpRouterFactoryOptions = {
+  /**
+   * The path to forward all unmatched requests to. Defaults to '/api/app'
+   */
+  indexPath?: string | false;
+
+  /**
+   * Middlewares that are added before all other routes.
+   */
+  middleware?: Handler[];
+};
+
+/** @public */
+export const rootHttpRouterFactory = createServiceFactory({
+  service: coreServices.rootHttpRouter,
+  deps: {
+    config: coreServices.config,
+    lifecycle: coreServices.rootLifecycle,
+  },
+  async factory({ config, lifecycle }, options?: RootHttpRouterFactoryOptions) {
+    const indexPath = options?.indexPath ?? '/api/app';
+
+    const namedRouter = Router();
+    const indexRouter = Router();
+
+    const service = createServiceBuilder(module).loadConfig(config);
+
+    for (const middleware of options?.middleware ?? []) {
+      service.addRouter('', middleware);
+    }
+
+    service.addRouter('', namedRouter).addRouter('', indexRouter);
+
+    const server = await service.start();
+    // Stop method isn't part of the public API, let's fix that once we move the implementation here.
+    const stoppableServer = server as typeof server & {
+      stop: (cb: (error?: Error) => void) => void;
+    };
+
+    lifecycle.addShutdownHook({
+      async fn() {
+        await new Promise<void>((resolve, reject) => {
+          stoppableServer.stop((error?: Error) => {
+            if (error) {
+              reject(error);
+            } else {
+              resolve();
+            }
+          });
+        });
+      },
+      labels: { service: 'rootHttpRouter' },
+    });
+
+    const existingPaths = new Array<string>();
+
+    return {
+      use: (path: string, handler: Handler) => {
+        if (path.match(/^[/\s]*$/)) {
+          throw new Error(`Root router path may not be empty`);
+        }
+        const conflictingPath = findConflictingPath(existingPaths, path);
+        if (conflictingPath) {
+          throw new Error(
+            `Path ${path} conflicts with the existing path ${conflictingPath}`,
+          );
+        }
+        existingPaths.push(path);
+        namedRouter.use(path, handler);
+
+        if (indexPath === path) {
+          indexRouter.use(handler);
+        }
+      },
+    };
+  },
+});
+
+function normalizePath(path: string): string {
+  return path.replace(/\/*$/, '/');
+}
+
+export function findConflictingPath(
+  paths: string[],
+  newPath: string,
+): string | undefined {
+  const normalizedNewPath = normalizePath(newPath);
+  for (const path of paths) {
+    const normalizedPath = normalizePath(path);
+    if (normalizedPath.startsWith(normalizedNewPath)) {
+      return path;
+    }
+    if (normalizedNewPath.startsWith(normalizedPath)) {
+      return path;
+    }
+  }
+  return undefined;
+}
diff --git a/packages/backend-defaults/src/CreateBackend.ts b/packages/backend-defaults/src/CreateBackend.ts
index a37a8c32b2..20edfc85a8 100644
--- a/packages/backend-defaults/src/CreateBackend.ts
+++ b/packages/backend-defaults/src/CreateBackend.ts
@@ -22,6 +22,7 @@ import {
   databaseFactory,
   discoveryFactory,
   httpRouterFactory,
+  rootHttpRouterFactory,
   lifecycleFactory,
   rootLifecycleFactory,
   loggerFactory,
@@ -45,6 +46,7 @@ export const defaultServiceFactories = [
   tokenManagerFactory,
   urlReaderFactory,
   httpRouterFactory,
+  rootHttpRouterFactory,
   lifecycleFactory,
   rootLifecycleFactory,
 ];
diff --git a/packages/backend-plugin-api/api-report.md b/packages/backend-plugin-api/api-report.md
index 16f00ad89f..3ec60bde46 100644
--- a/packages/backend-plugin-api/api-report.md
+++ b/packages/backend-plugin-api/api-report.md
@@ -80,6 +80,7 @@ export namespace coreServices {
   const logger: ServiceRef<LoggerService, 'plugin'>;
   const permissions: ServiceRef<PermissionsService, 'plugin'>;
   const pluginMetadata: ServiceRef<PluginMetadataService, 'plugin'>;
+  const rootHttpRouter: ServiceRef<RootHttpRouterService, 'root'>;
   const rootLifecycle: ServiceRef<RootLifecycleService, 'root'>;
   const rootLogger: ServiceRef<RootLoggerService, 'root'>;
   const scheduler: ServiceRef<SchedulerService, 'plugin'>;
@@ -257,6 +258,11 @@ export type ReadUrlResponse = {
   etag?: string;
 };
 
+// @public (undocumented)
+export interface RootHttpRouterService {
+  use(path: string, handler: Handler): void;
+}
+
 // @public (undocumented)
 export interface RootLifecycleService extends LifecycleService {}
 
diff --git a/packages/backend-plugin-api/src/services/definitions/RootHttpRouterService.ts b/packages/backend-plugin-api/src/services/definitions/RootHttpRouterService.ts
new file mode 100644
index 0000000000..e583e978fa
--- /dev/null
+++ b/packages/backend-plugin-api/src/services/definitions/RootHttpRouterService.ts
@@ -0,0 +1,28 @@
+/*
+ * Copyright 2022 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 { Handler } from 'express';
+
+/**
+ * @public
+ */
+export interface RootHttpRouterService {
+  /**
+   * Registers a handler at the root of the backend router.
+   * The path is required and may not be empty.
+   */
+  use(path: string, handler: Handler): void;
+}
diff --git a/packages/backend-plugin-api/src/services/definitions/coreServices.ts b/packages/backend-plugin-api/src/services/definitions/coreServices.ts
index fc96ec8be9..7de92d6d01 100644
--- a/packages/backend-plugin-api/src/services/definitions/coreServices.ts
+++ b/packages/backend-plugin-api/src/services/definitions/coreServices.ts
@@ -103,6 +103,15 @@ export namespace coreServices {
     import('./PluginMetadataService').PluginMetadataService
   >({ id: 'core.pluginMetadata' });
 
+  /**
+   * The service reference for the root scoped {@link RootHttpRouterService}.
+   *
+   * @public
+   */
+  export const rootHttpRouter = createServiceRef<
+    import('./RootHttpRouterService').RootHttpRouterService
+  >({ id: 'core.rootHttpRouter', scope: 'root' });
+
   /**
    * The service reference for the root scoped {@link RootLifecycleService}.
    *
diff --git a/packages/backend-plugin-api/src/services/definitions/index.ts b/packages/backend-plugin-api/src/services/definitions/index.ts
index dedfd6223e..82b16efda2 100644
--- a/packages/backend-plugin-api/src/services/definitions/index.ts
+++ b/packages/backend-plugin-api/src/services/definitions/index.ts
@@ -27,6 +27,7 @@ export type {
 export type { LoggerService, LogMeta } from './LoggerService';
 export type { PermissionsService } from './PermissionsService';
 export type { PluginMetadataService } from './PluginMetadataService';
+export type { RootHttpRouterService } from './RootHttpRouterService';
 export type { RootLifecycleService } from './RootLifecycleService';
 export type { RootLoggerService } from './RootLoggerService';
 export type { SchedulerService } from './SchedulerService';
diff --git a/plugins/app-backend/src/service/appPlugin.test.ts b/plugins/app-backend/src/service/appPlugin.test.ts
index 14921622c9..80408694d6 100644
--- a/plugins/app-backend/src/service/appPlugin.test.ts
+++ b/plugins/app-backend/src/service/appPlugin.test.ts
@@ -23,6 +23,7 @@ import { appPlugin } from './appPlugin';
 import {
   databaseFactory,
   httpRouterFactory,
+  rootHttpRouterFactory,
   loggerFactory,
   rootLoggerFactory,
 } from '@backstage/backend-app-api';
@@ -63,6 +64,7 @@ describe('appPlugin', () => {
         rootLoggerFactory(),
         databaseFactory(),
         httpRouterFactory(),
+        rootHttpRouterFactory(),
       ],
       features: [
         appPlugin({
diff --git a/yarn.lock b/yarn.lock
index 44a2b9f9b2..6c74158f04 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -3382,6 +3382,7 @@ __metadata:
     "@backstage/cli": "workspace:^"
     "@backstage/errors": "workspace:^"
     "@backstage/plugin-permission-node": "workspace:^"
+    "@types/express": ^4.17.6
     express: ^4.17.1
     express-promise-router: ^4.1.0
     winston: ^3.2.1