diff --git a/.changeset/tame-clouds-confess.md b/.changeset/tame-clouds-confess.md
new file mode 100644
index 0000000000..05af248eb1
--- /dev/null
+++ b/.changeset/tame-clouds-confess.md
@@ -0,0 +1,5 @@
+---
+'@backstage/core-api': patch
+---
+
+Wait for `configApi` to be ready before using `featureFlagsApi`
diff --git a/packages/core-api/src/app/App.test.tsx b/packages/core-api/src/app/App.test.tsx
index a9f1e81a11..8f4847c2f0 100644
--- a/packages/core-api/src/app/App.test.tsx
+++ b/packages/core-api/src/app/App.test.tsx
@@ -14,6 +14,12 @@
  * limitations under the License.
  */
 
+import {
+  configApiRef,
+  createApiFactory,
+  featureFlagsApiRef,
+  LocalStorageFeatureFlags,
+} from '../apis';
 import { renderWithEffects, withLogCollector } from '@backstage/test-utils';
 import { lightTheme } from '@backstage/theme';
 import { render, screen } from '@testing-library/react';
@@ -245,6 +251,67 @@ describe('Integration Test', () => {
     expect(screen.getByText('extLink4: <none>')).toBeInTheDocument();
   });
 
+  it('should wait for the config to load before calling feature flags', async () => {
+    const storageFlags = new LocalStorageFeatureFlags();
+    jest.spyOn(storageFlags, 'registerFlag');
+
+    const apis = [
+      createApiFactory({
+        api: featureFlagsApiRef,
+        deps: { configApi: configApiRef },
+        factory() {
+          return storageFlags;
+        },
+      }),
+    ];
+
+    const app = new PrivateAppImpl({
+      apis,
+      defaultApis: [],
+      themes: [
+        {
+          id: 'light',
+          title: 'Light Theme',
+          variant: 'light',
+          theme: lightTheme,
+        },
+      ],
+      icons: defaultSystemIcons,
+      plugins: [
+        createPlugin({
+          id: 'test',
+          register: p => p.featureFlags.register('name'),
+        }),
+      ],
+      components,
+      bindRoutes: ({ bind }) => {
+        bind(plugin1.externalRoutes, {
+          err: plugin1RouteRef,
+          errParams: plugin2RouteRef,
+        });
+      },
+    });
+
+    const Provider = app.getProvider();
+    const Router = app.getRouter();
+
+    await renderWithEffects(
+      <Provider>
+        <Router>
+          <Routes>
+            <ExposedComponent path="/" />
+            <HiddenComponent path="/foo" />
+          </Routes>
+        </Router>
+      </Provider>,
+    );
+
+    expect(storageFlags.registerFlag).toHaveBeenCalledWith({
+      name: 'name',
+      pluginId: 'test',
+    });
+  });
+
   it('should throw some error when the route has duplicate params', () => {
     const app = new PrivateAppImpl({
       apis: [],
diff --git a/packages/core-api/src/app/App.tsx b/packages/core-api/src/app/App.tsx
index 9e14c9a5fb..c20eb0824e 100644
--- a/packages/core-api/src/app/App.tsx
+++ b/packages/core-api/src/app/App.tsx
@@ -14,10 +14,12 @@
  * limitations under the License.
  */
 
+import { Config } from '@backstage/config';
 import React, {
   ComponentType,
   PropsWithChildren,
   ReactElement,
+  useEffect,
   useMemo,
   useState,
 } from 'react';
@@ -278,24 +280,6 @@ export class PrivateAppImpl implements BackstageApp {
     const appContext = new AppContextImpl(this);
     const apiHolder = this.getApiHolder();
 
-    const featureFlagsApi = this.getApiHolder().get(featureFlagsApiRef)!;
-
-    for (const plugin of this.plugins.values()) {
-      for (const output of plugin.output()) {
-        switch (output.type) {
-          case 'feature-flag': {
-            featureFlagsApi.registerFlag({
-              name: output.name,
-              pluginId: plugin.getId(),
-            });
-            break;
-          }
-          default:
-            break;
-        }
-      }
-    }
-
     const Provider = ({ children }: PropsWithChildren<{}>) => {
       const appThemeApi = useMemo(
         () => AppThemeSelector.createWithStorage(this.themes),
@@ -324,13 +308,39 @@ export class PrivateAppImpl implements BackstageApp {
         appThemeApi,
       );
 
+      const hasConfigApi = 'api' in loadedConfig;
+      if (hasConfigApi) {
+        const { api } = loadedConfig as { api: Config };
+        this.configApi = api;
+      }
+
+      useEffect(() => {
+        if (hasConfigApi) {
+          const featureFlagsApi = this.getApiHolder().get(featureFlagsApiRef)!;
+
+          for (const plugin of this.plugins.values()) {
+            for (const output of plugin.output()) {
+              switch (output.type) {
+                case 'feature-flag': {
+                  featureFlagsApi.registerFlag({
+                    name: output.name,
+                    pluginId: plugin.getId(),
+                  });
+                  break;
+                }
+                default:
+                  break;
+              }
+            }
+          }
+        }
+      }, [hasConfigApi, loadedConfig]);
+
       if ('node' in loadedConfig) {
         // Loading or error
         return loadedConfig.node;
       }
 
-      this.configApi = loadedConfig.api;
-
       return (
         <ApiProvider apis={apiHolder}>
           <AppContextProvider appContext={appContext}>