diff --git a/packages/dev-middleware/src/inspector-proxy/types.js b/packages/dev-middleware/src/inspector-proxy/types.js
index a89bfc9a914d..ed37c285fc5a 100644
--- a/packages/dev-middleware/src/inspector-proxy/types.js
+++ b/packages/dev-middleware/src/inspector-proxy/types.js
@@ -37,6 +37,13 @@ export type TargetCapabilityFlags = $ReadOnly<{
    * In the proxy, this disables intercepting and storing network requests.
    */
   nativeNetworkInspection?: boolean,
+
+  /**
+   * The target supports the modern `rn_fusebox.html` entry point.
+   *
+   * In the launch flow, this controls the Chrome DevTools entrypoint that is used.
+   */
+  prefersFuseboxFrontend?: boolean,
 }>;
 
 // Page information received from the device. New page is created for
diff --git a/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js b/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
index 6b571f7aa026..2f1cf95b5d15 100644
--- a/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
+++ b/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
@@ -107,6 +107,9 @@ export default function openDebuggerMiddleware({
         return;
       }
 
+      const useFuseboxEntryPoint =
+        target.reactNative.capabilities?.prefersFuseboxFrontend;
+
       try {
         switch (launchType) {
           case 'launch':
@@ -122,6 +125,7 @@ export default function openDebuggerMiddleware({
                   experiments,
                   target.webSocketDebuggerUrl,
                   serverBaseUrl,
+                  {useFuseboxEntryPoint},
                 ),
               ),
             );
@@ -133,7 +137,7 @@ export default function openDebuggerMiddleware({
                 experiments,
                 target.webSocketDebuggerUrl,
                 serverBaseUrl,
-                {relative: true},
+                {relative: true, useFuseboxEntryPoint},
               ),
             });
             res.end();
diff --git a/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js b/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
index 7dd33dfd9d08..a3cabc78afc0 100644
--- a/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
+++ b/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
@@ -20,6 +20,7 @@ export default function getDevToolsFrontendUrl(
   devServerUrl: string,
   options?: $ReadOnly<{
     relative?: boolean,
+    useFuseboxEntryPoint?: boolean,
   }>,
 ): string {
   const wsParam = getWsParam({
@@ -29,7 +30,10 @@ export default function getDevToolsFrontendUrl(
 
   const appUrl =
     (options?.relative === true ? '' : devServerUrl) +
-    '/debugger-frontend/rn_inspector.html';
+    '/debugger-frontend/' +
+    (options?.useFuseboxEntryPoint === true
+      ? 'rn_fusebox.html'
+      : 'rn_inspector.html');
 
   const searchParams = new URLSearchParams([
     [wsParam.key, wsParam.value],
diff --git a/packages/react-native/React/Base/RCTBridge.mm b/packages/react-native/React/Base/RCTBridge.mm
index 0a5e8a6dc899..5ffcb25d8879 100644
--- a/packages/react-native/React/Base/RCTBridge.mm
+++ b/packages/react-native/React/Base/RCTBridge.mm
@@ -436,7 +436,7 @@ - (void)setUp
                   .integrationName = "iOS Bridge (RCTBridge)",
               });
         },
-        {.nativePageReloads = true});
+        {.nativePageReloads = true, .prefersFuseboxFrontend = true});
   }
 
   Class bridgeClass = self.bridgeClass;
diff --git a/packages/react-native/ReactAndroid/src/main/jni/react/jni/ReactInstanceManagerInspectorTarget.cpp b/packages/react-native/ReactAndroid/src/main/jni/react/jni/ReactInstanceManagerInspectorTarget.cpp
index 52e1b8795933..aba0a4335ada 100644
--- a/packages/react-native/ReactAndroid/src/main/jni/react/jni/ReactInstanceManagerInspectorTarget.cpp
+++ b/packages/react-native/ReactAndroid/src/main/jni/react/jni/ReactInstanceManagerInspectorTarget.cpp
@@ -50,7 +50,7 @@ ReactInstanceManagerInspectorTarget::ReactInstanceManagerInspectorTarget(
                       "Android Bridge (ReactInstanceManagerInspectorTarget)",
               });
         },
-        {.nativePageReloads = true});
+        {.nativePageReloads = true, .prefersFuseboxFrontend = true});
   }
 }
 
diff --git a/packages/react-native/ReactAndroid/src/main/jni/react/runtime/jni/JReactHostInspectorTarget.cpp b/packages/react-native/ReactAndroid/src/main/jni/react/runtime/jni/JReactHostInspectorTarget.cpp
index eb47f4af4a32..89fd8ce02bb9 100644
--- a/packages/react-native/ReactAndroid/src/main/jni/react/runtime/jni/JReactHostInspectorTarget.cpp
+++ b/packages/react-native/ReactAndroid/src/main/jni/react/runtime/jni/JReactHostInspectorTarget.cpp
@@ -45,7 +45,7 @@ JReactHostInspectorTarget::JReactHostInspectorTarget(
           // Reject the connection.
           return nullptr;
         },
-        {.nativePageReloads = true});
+        {.nativePageReloads = true, .prefersFuseboxFrontend = true});
   }
 }
 
diff --git a/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.cpp b/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.cpp
index b8ac15d7b919..295805593899 100644
--- a/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.cpp
+++ b/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.cpp
@@ -28,7 +28,8 @@ const folly::dynamic targetCapabilitiesToDynamic(
     const InspectorTargetCapabilities& capabilities) {
   return folly::dynamic::object(
       "nativePageReloads", capabilities.nativePageReloads)(
-      "nativeSourceCodeFetching", capabilities.nativeSourceCodeFetching);
+      "nativeSourceCodeFetching", capabilities.nativeSourceCodeFetching)(
+      "prefersFuseboxFrontend", capabilities.prefersFuseboxFrontend);
 }
 
 namespace {
diff --git a/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.h b/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.h
index 07591f194d57..5790c059b45d 100644
--- a/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.h
+++ b/packages/react-native/ReactCommon/jsinspector-modern/InspectorInterfaces.h
@@ -36,6 +36,7 @@ class IDestructible {
 struct InspectorTargetCapabilities {
   const bool nativePageReloads = false;
   const bool nativeSourceCodeFetching = false;
+  const bool prefersFuseboxFrontend = false;
 };
 
 const folly::dynamic targetCapabilitiesToDynamic(
diff --git a/packages/react-native/ReactCommon/react/runtime/platform/ios/ReactCommon/RCTHost.mm b/packages/react-native/ReactCommon/react/runtime/platform/ios/ReactCommon/RCTHost.mm
index 4547a0daee19..975906420bf1 100644
--- a/packages/react-native/ReactCommon/react/runtime/platform/ios/ReactCommon/RCTHost.mm
+++ b/packages/react-native/ReactCommon/react/runtime/platform/ios/ReactCommon/RCTHost.mm
@@ -191,7 +191,7 @@ - (void)start
                   .integrationName = "iOS Bridgeless (RCTHost)",
               });
         },
-        {.nativePageReloads = true});
+        {.nativePageReloads = true, .prefersFuseboxFrontend = true});
   }
   if (_instance) {
     RCTLogWarn(