diff --git a/.changeset/gentle-ligers-help.md b/.changeset/gentle-ligers-help.md
new file mode 100644
index 0000000000..f7f9c3b270
--- /dev/null
+++ b/.changeset/gentle-ligers-help.md
@@ -0,0 +1,5 @@
+---
+'@backstage/core-app-api': patch
+---
+
+Tweak feature flag registration so that it happens immediately before the first rendering of the app, rather than just after.
diff --git a/packages/core-app-api/src/app/AppManager.test.tsx b/packages/core-app-api/src/app/AppManager.test.tsx
index df3d6f5a27..17d33693e5 100644
--- a/packages/core-app-api/src/app/AppManager.test.tsx
+++ b/packages/core-app-api/src/app/AppManager.test.tsx
@@ -34,6 +34,7 @@ import {
   createSubRouteRef,
   createRoutableExtension,
   analyticsApiRef,
+  useApi,
 } from '@backstage/core-plugin-api';
 import { AppManager } from './AppManager';
 import { AppComponents, AppIcons } from './types';
@@ -395,6 +396,44 @@ describe('Integration Test', () => {
     });
   });
 
+  it('feature flags should be available immediately', async () => {
+    const app = new AppManager({
+      apis: [
+        createApiFactory({
+          api: featureFlagsApiRef,
+          deps: { configApi: configApiRef },
+          factory() {
+            return new LocalStorageFeatureFlags();
+          },
+        }),
+      ],
+      defaultApis: [],
+      themes,
+      icons,
+      plugins: [createPlugin({ id: 'test', featureFlags: [{ name: 'foo' }] })],
+      components,
+      configLoader: async () => [],
+    });
+
+    const Provider = app.getProvider();
+    const Router = app.getRouter();
+
+    const FeatureFlags = () => {
+      const featureFlags = useApi(featureFlagsApiRef).getRegisteredFlags();
+      return <div>Flags: {featureFlags.map(f => f.name).join(',')}</div>;
+    };
+
+    await renderWithEffects(
+      <Provider>
+        <Router>
+          <FeatureFlags />
+        </Router>
+      </Provider>,
+    );
+
+    expect(screen.getByText('Flags: foo')).toBeInTheDocument();
+  });
+
   it('should track route changes via analytics api', async () => {
     const mockAnalyticsApi = new MockAnalyticsApi();
     const apis = [createApiFactory(analyticsApiRef, mockAnalyticsApi)];
diff --git a/packages/core-app-api/src/app/AppManager.tsx b/packages/core-app-api/src/app/AppManager.tsx
index 4582a3c7cd..a6e15fe40c 100644
--- a/packages/core-app-api/src/app/AppManager.tsx
+++ b/packages/core-app-api/src/app/AppManager.tsx
@@ -21,8 +21,8 @@ import React, {
   PropsWithChildren,
   ReactElement,
   useContext,
-  useEffect,
   useMemo,
+  useRef,
   useState,
 } from 'react';
 import { Route, Routes } from 'react-router-dom';
@@ -230,6 +230,7 @@ export class AppManager implements BackstageApp {
     let routesHaveBeenValidated = false;
 
     const Provider = ({ children }: PropsWithChildren<{}>) => {
+      const needsFeatureFlagRegistrationRef = useRef(true);
       const appThemeApi = useMemo(
         () => AppThemeSelector.createWithStorage(this.themes),
         [],
@@ -284,10 +285,21 @@ export class AppManager implements BackstageApp {
         this.configApi = api;
       }
 
-      useEffect(() => {
-        if (hasConfigApi) {
-          const featureFlagsApi = this.getApiHolder().get(featureFlagsApiRef)!;
+      if ('node' in loadedConfig) {
+        // Loading or error
+        return loadedConfig.node;
+      }
 
+      // We can't register feature flags just after the element traversal, because the
+      // config API isn't available yet and implementations frequently depend on it.
+      // Instead we make it happen immediately, to make sure all flags are available
+      // for the first render.
+      if (hasConfigApi && needsFeatureFlagRegistrationRef.current) {
+        needsFeatureFlagRegistrationRef.current = false;
+
+        const featureFlagsApi = this.getApiHolder().get(featureFlagsApiRef)!;
+
+        if (featureFlagsApi) {
           for (const plugin of this.plugins.values()) {
             if ('getFeatureFlags' in plugin) {
               for (const flag of plugin.getFeatureFlags()) {
@@ -314,11 +326,6 @@ export class AppManager implements BackstageApp {
             featureFlagsApi.registerFlag({ name, pluginId: '' });
           }
         }
-      }, [hasConfigApi, loadedConfig, featureFlags]);
-
-      if ('node' in loadedConfig) {
-        // Loading or error
-        return loadedConfig.node;
       }
 
       const { ThemeProvider = AppThemeProvider } = this.components;