diff --git a/packages/metro-config/src/__tests__/__snapshots__/loadConfig-test.js.snap b/packages/metro-config/src/__tests__/__snapshots__/loadConfig-test.js.snap
index 5156df2dbb..89f21b7fb6 100644
--- a/packages/metro-config/src/__tests__/__snapshots__/loadConfig-test.js.snap
+++ b/packages/metro-config/src/__tests__/__snapshots__/loadConfig-test.js.snap
@@ -101,6 +101,7 @@ Object {
     "enhanceMiddleware": [Function],
     "port": 8081,
     "rewriteRequestUrl": [Function],
+    "runInspectorProxy": true,
     "unstable_serverRoot": null,
     "useGlobalHotkey": true,
     "verifyConnections": false,
@@ -278,6 +279,7 @@ Object {
     "enhanceMiddleware": [Function],
     "port": 8081,
     "rewriteRequestUrl": [Function],
+    "runInspectorProxy": true,
     "unstable_serverRoot": null,
     "useGlobalHotkey": true,
     "verifyConnections": false,
@@ -455,6 +457,7 @@ Object {
     "enhanceMiddleware": [Function],
     "port": 8081,
     "rewriteRequestUrl": [Function],
+    "runInspectorProxy": true,
     "unstable_serverRoot": null,
     "useGlobalHotkey": true,
     "verifyConnections": false,
@@ -632,6 +635,7 @@ Object {
     "enhanceMiddleware": [Function],
     "port": 8081,
     "rewriteRequestUrl": [Function],
+    "runInspectorProxy": true,
     "unstable_serverRoot": null,
     "useGlobalHotkey": true,
     "verifyConnections": false,
diff --git a/packages/metro-config/src/configTypes.flow.js b/packages/metro-config/src/configTypes.flow.js
index 6dafad4ea4..29542dd352 100644
--- a/packages/metro-config/src/configTypes.flow.js
+++ b/packages/metro-config/src/configTypes.flow.js
@@ -168,6 +168,7 @@ type ServerConfigT = {
   enhanceMiddleware: (Middleware, MetroServer) => Middleware | Server,
   port: number,
   rewriteRequestUrl: string => string,
+  runInspectorProxy: boolean,
   unstable_serverRoot: ?string,
   useGlobalHotkey: boolean,
   verifyConnections: boolean,
@@ -261,6 +262,7 @@ export type YargArguments = $ReadOnly<{
   transformer?: string,
   'reset-cache'?: boolean,
   resetCache?: boolean,
+  runInspectorProxy?: boolean,
   verbose?: boolean,
   ...
 }>;
diff --git a/packages/metro-config/src/defaults/index.js b/packages/metro-config/src/defaults/index.js
index 86c9be1f75..e30928c8c1 100644
--- a/packages/metro-config/src/defaults/index.js
+++ b/packages/metro-config/src/defaults/index.js
@@ -76,6 +76,7 @@ const getDefaultValues = (projectRoot: ?string): ConfigT => ({
     enhanceMiddleware: (middleware, _) => middleware,
     port: 8081,
     rewriteRequestUrl: url => url,
+    runInspectorProxy: true,
     unstable_serverRoot: null,
     useGlobalHotkey: true,
     verifyConnections: false,
diff --git a/packages/metro-config/src/loadConfig.js b/packages/metro-config/src/loadConfig.js
index d2c65b0438..22517d5714 100644
--- a/packages/metro-config/src/loadConfig.js
+++ b/packages/metro-config/src/loadConfig.js
@@ -234,6 +234,12 @@ function overrideConfigWithArguments(
     output.server.port = Number(argv.port);
   }
 
+  if (argv.runInspectorProxy != null) {
+    // $FlowFixMe[incompatible-use]
+    // $FlowFixMe[cannot-write]
+    output.server.runInspectorProxy = Boolean(argv.runInspectorProxy);
+  }
+
   if (argv.projectRoot != null) {
     output.projectRoot = argv.projectRoot;
   }
diff --git a/packages/metro-config/types/configTypes.d.ts b/packages/metro-config/types/configTypes.d.ts
index 8d6e0d6721..c4a89aabdf 100644
--- a/packages/metro-config/types/configTypes.d.ts
+++ b/packages/metro-config/types/configTypes.d.ts
@@ -166,6 +166,7 @@ export interface ServerConfigT {
   ) => Middleware | Server;
   port: number;
   rewriteRequestUrl: (url: string) => string;
+  runInspectorProxy: boolean;
   unstable_serverRoot: string | null;
   useGlobalHotkey: boolean;
   verifyConnections: boolean;
@@ -250,5 +251,6 @@ export interface YargArguments {
   transformer?: string;
   'reset-cache'?: boolean;
   resetCache?: boolean;
+  runInspectorProxy?: boolean;
   verbose?: boolean;
 }
diff --git a/packages/metro/package.json b/packages/metro/package.json
index 15509b9aa5..f1941a2f8d 100644
--- a/packages/metro/package.json
+++ b/packages/metro/package.json
@@ -41,6 +41,7 @@
     "metro-config": "0.78.0",
     "metro-core": "0.78.0",
     "metro-file-map": "0.78.0",
+    "metro-inspector-proxy": "0.78.0",
     "metro-minify-terser": "0.78.0",
     "metro-resolver": "0.78.0",
     "metro-runtime": "0.78.0",
diff --git a/packages/metro/src/index.flow.js b/packages/metro/src/index.flow.js
index 0e751e7788..4ba27a4db3 100644
--- a/packages/metro/src/index.flow.js
+++ b/packages/metro/src/index.flow.js
@@ -47,6 +47,7 @@ const {
   resolveConfig,
 } = require('metro-config');
 const {Terminal} = require('metro-core');
+const {InspectorProxy} = require('metro-inspector-proxy');
 const net = require('net');
 const {parse} = require('url');
 
@@ -67,6 +68,7 @@ export type RunServerOptions = $ReadOnly<{
   host?: string,
   onError?: (Error & {code?: string}) => void,
   onReady?: (server: HttpServer | HttpsServer) => void,
+  runInspectorProxy?: boolean,
   secureServerOptions?: Object,
   secure?: boolean, // deprecated
   secureCert?: string, // deprecated
@@ -279,6 +281,11 @@ exports.runServer = async (
     serverApp.use(handler);
   }
 
+  let inspectorProxy: ?InspectorProxy = null;
+  if (config.server.runInspectorProxy) {
+    inspectorProxy = new InspectorProxy(config.projectRoot);
+  }
+
   let httpServer;
 
   if (secure || secureServerOptions != null) {
@@ -315,6 +322,9 @@ exports.runServer = async (
 
         websocketEndpoints = {
           ...websocketEndpoints,
+          ...(inspectorProxy
+            ? {...inspectorProxy.createWebSocketListeners(httpServer)}
+            : {}),
           '/hot': createWebsocketServer({
             websocketServer: new MetroHmrServer(
               metroServer.getBundler(),
@@ -340,6 +350,14 @@ exports.runServer = async (
           }
         });
 
+        if (inspectorProxy) {
+          // TODO(hypuk): Refactor inspectorProxy.processRequest into separate request handlers
+          // so that we could provide routes (/json/list and /json/version) here.
+          // Currently this causes Metro to give warning about T31407894.
+          // $FlowFixMe[method-unbinding] added when improving typing for this parameters
+          serverApp.use(inspectorProxy.processRequest.bind(inspectorProxy));
+        }
+
         resolve(httpServer);
       });
 
diff --git a/packages/metro/types/index.d.ts b/packages/metro/types/index.d.ts
index 62dee34c60..8238e20145 100644
--- a/packages/metro/types/index.d.ts
+++ b/packages/metro/types/index.d.ts
@@ -62,6 +62,7 @@ export interface RunServerOptions {
   host?: string;
   onError?: (error: Error & {code?: string}) => void;
   onReady?: (server: HttpServer | HttpsServer) => void;
+  runInspectorProxy?: boolean;
   secureServerOptions?: Record<string, unknown>;
 
   /** @deprecated since version 0.61 */