diff --git a/packages/dev-middleware/src/__tests__/getDevToolsFrontendUrl-test.js b/packages/dev-middleware/src/__tests__/getDevToolsFrontendUrl-test.js
index 3d0818efc25760..a6fe45b710bf8a 100644
--- a/packages/dev-middleware/src/__tests__/getDevToolsFrontendUrl-test.js
+++ b/packages/dev-middleware/src/__tests__/getDevToolsFrontendUrl-test.js
@@ -14,16 +14,16 @@ import getDevToolsFrontendUrl from '../utils/getDevToolsFrontendUrl';
 describe('getDevToolsFrontendUrl', () => {
   const webSocketDebuggerUrl =
     'ws://localhost:8081/inspector/debug?device=1a9372c&page=-1';
+  const devServerUrl = 'http://localhost:8081';
 
-  describe('given an absolute devServerUrl', () => {
-    const devServerUrl = 'http://localhost:8081';
+  const experiments = {
+    enableNetworkInspector: false,
+    enableNewDebugger: false,
+    enableOpenDebuggerRedirect: false,
+  };
 
-    it('should return a valid url for all experiments off', async () => {
-      const experiments = {
-        enableNetworkInspector: false,
-        enableNewDebugger: false,
-        enableOpenDebuggerRedirect: false,
-      };
+  describe('relative: false (default)', () => {
+    test('should return a valid url for all experiments off', async () => {
       const actual = getDevToolsFrontendUrl(
         experiments,
         webSocketDebuggerUrl,
@@ -33,18 +33,13 @@ describe('getDevToolsFrontendUrl', () => {
       expect(url.host).toBe('localhost:8081');
       expect(url.pathname).toBe('/debugger-frontend/rn_inspector.html');
       expect(url.searchParams.get('ws')).toBe(
-        'localhost:8081/inspector/debug?device=1a9372c&page=-1',
+        '/inspector/debug?device=1a9372c&page=-1',
       );
     });
 
-    it('should return a valid url for enableNetworkInspector experiment on', async () => {
-      const experiments = {
-        enableNetworkInspector: true,
-        enableNewDebugger: true,
-        enableOpenDebuggerRedirect: false,
-      };
+    test('should return a valid url for enableNetworkInspector experiment on', async () => {
       const actual = getDevToolsFrontendUrl(
-        experiments,
+        {...experiments, enableNetworkInspector: true, enableNewDebugger: true},
         webSocketDebuggerUrl,
         devServerUrl,
       );
@@ -53,14 +48,26 @@ describe('getDevToolsFrontendUrl', () => {
       expect(url.pathname).toBe('/debugger-frontend/rn_inspector.html');
       expect(url.searchParams.get('unstable_enableNetworkPanel')).toBe('true');
       expect(url.searchParams.get('ws')).toBe(
-        'localhost:8081/inspector/debug?device=1a9372c&page=-1',
+        '/inspector/debug?device=1a9372c&page=-1',
       );
     });
-  });
 
-  describe('given a relative devServerUrl', () => {
-    const relativeDevServerUrl = '';
+    test('should return a full WS URL if on a different host than the dev server', () => {
+      const otherWebSocketDebuggerUrl =
+        'ws://localhost:9000/inspector/debug?device=1a9372c&page=-1';
+      const actual = getDevToolsFrontendUrl(
+        experiments,
+        otherWebSocketDebuggerUrl,
+        devServerUrl,
+      );
+      const url = new URL(actual);
+      expect(url.searchParams.get('ws')).toBe(
+        'localhost:9000/inspector/debug?device=1a9372c&page=-1',
+      );
+    });
+  });
 
+  describe('relative: true', () => {
     function assertValidRelativeURL(relativeURL: string): URL {
       const anyBaseURL = new URL('https://www.example.com');
       try {
@@ -71,40 +78,53 @@ describe('getDevToolsFrontendUrl', () => {
       }
     }
 
-    it('should return a valid url for all experiments off', async () => {
-      const experiments = {
-        enableNetworkInspector: false,
-        enableNewDebugger: false,
-        enableOpenDebuggerRedirect: false,
-      };
+    test('should return a valid url for all experiments off', async () => {
       const actual = getDevToolsFrontendUrl(
         experiments,
         webSocketDebuggerUrl,
-        relativeDevServerUrl,
+        devServerUrl,
+        {
+          relative: true,
+        },
       );
       const url = assertValidRelativeURL(actual);
       expect(url.pathname).toBe('/debugger-frontend/rn_inspector.html');
       expect(url.searchParams.get('ws')).toBe(
-        'localhost:8081/inspector/debug?device=1a9372c&page=-1',
+        '/inspector/debug?device=1a9372c&page=-1',
       );
     });
 
-    it('should return a valid url for enableNetworkInspector experiment on', async () => {
-      const experiments = {
-        enableNetworkInspector: true,
-        enableNewDebugger: true,
-        enableOpenDebuggerRedirect: false,
-      };
+    test('should return a valid url for enableNetworkInspector experiment on', async () => {
       const actual = getDevToolsFrontendUrl(
-        experiments,
+        {...experiments, enableNetworkInspector: true, enableNewDebugger: true},
         webSocketDebuggerUrl,
-        relativeDevServerUrl,
+        devServerUrl,
+        {
+          relative: true,
+        },
       );
       const url = assertValidRelativeURL(actual);
       expect(url.pathname).toBe('/debugger-frontend/rn_inspector.html');
       expect(url.searchParams.get('unstable_enableNetworkPanel')).toBe('true');
       expect(url.searchParams.get('ws')).toBe(
-        'localhost:8081/inspector/debug?device=1a9372c&page=-1',
+        '/inspector/debug?device=1a9372c&page=-1',
+      );
+    });
+
+    test('should return a full WS URL if on a different host than the dev server', () => {
+      const otherWebSocketDebuggerUrl =
+        'ws://localhost:8082/inspector/debug?device=1a9372c&page=-1';
+      const actual = getDevToolsFrontendUrl(
+        experiments,
+        otherWebSocketDebuggerUrl,
+        devServerUrl,
+        {
+          relative: true,
+        },
+      );
+      const url = assertValidRelativeURL(actual);
+      expect(url.searchParams.get('ws')).toBe(
+        'localhost:8082/inspector/debug?device=1a9372c&page=-1',
       );
     });
   });
diff --git a/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js b/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
index 1f3b4d74358521..6b571f7aa026cd 100644
--- a/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
+++ b/packages/dev-middleware/src/middleware/openDebuggerMiddleware.js
@@ -132,8 +132,8 @@ export default function openDebuggerMiddleware({
               Location: getDevToolsFrontendUrl(
                 experiments,
                 target.webSocketDebuggerUrl,
-                // Use a relative URL.
-                '',
+                serverBaseUrl,
+                {relative: true},
               ),
             });
             res.end();
diff --git a/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js b/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
index 4623616292fea5..7dd33dfd9d08a3 100644
--- a/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
+++ b/packages/dev-middleware/src/utils/getDevToolsFrontendUrl.js
@@ -18,16 +18,21 @@ export default function getDevToolsFrontendUrl(
   experiments: Experiments,
   webSocketDebuggerUrl: string,
   devServerUrl: string,
+  options?: $ReadOnly<{
+    relative?: boolean,
+  }>,
 ): string {
-  const scheme = new URL(webSocketDebuggerUrl).protocol.slice(0, -1);
-  const webSocketUrlWithoutProtocol = webSocketDebuggerUrl.replace(
-    /^wss?:\/\//,
-    '',
-  );
-  const appUrl = `${devServerUrl}/debugger-frontend/rn_inspector.html`;
+  const wsParam = getWsParam({
+    webSocketDebuggerUrl,
+    devServerUrl,
+  });
+
+  const appUrl =
+    (options?.relative === true ? '' : devServerUrl) +
+    '/debugger-frontend/rn_inspector.html';
 
   const searchParams = new URLSearchParams([
-    [scheme, webSocketUrlWithoutProtocol],
+    [wsParam.key, wsParam.value],
     ['sources.hide_add_folder', 'true'],
   ]);
   if (experiments.enableNetworkInspector) {
@@ -36,3 +41,28 @@ export default function getDevToolsFrontendUrl(
 
   return appUrl + '?' + searchParams.toString();
 }
+
+function getWsParam({
+  webSocketDebuggerUrl,
+  devServerUrl,
+}: $ReadOnly<{
+  webSocketDebuggerUrl: string,
+  devServerUrl: string,
+}>): {
+  key: string,
+  value: string,
+} {
+  const wsUrl = new URL(webSocketDebuggerUrl);
+  const serverHost = new URL(devServerUrl).host;
+  let value;
+  if (wsUrl.host === serverHost) {
+    // Use a path-absolute (host-relative) URL
+    // Depends on https://github.com/facebookexperimental/rn-chrome-devtools-frontend/pull/4
+    value = wsUrl.pathname + wsUrl.search + wsUrl.hash;
+  } else {
+    // Standard URL format accepted by the DevTools frontend
+    value = wsUrl.host + wsUrl.pathname + wsUrl.search + wsUrl.hash;
+  }
+  const key = wsUrl.protocol.slice(0, -1);
+  return {key, value};
+}