diff --git a/devtools/shared/commands/target/target-command.js b/devtools/shared/commands/target/target-command.js
index afa1c5ec2c81..f0574868c401 100644
--- a/devtools/shared/commands/target/target-command.js
+++ b/devtools/shared/commands/target/target-command.js
@@ -266,6 +266,8 @@ class TargetCommand extends EventEmitter {
       const supportsWatcher = this.descriptorFront.traits?.watcher;
       if (supportsWatcher) {
         this.watcherFront = await this.descriptorFront.getWatcher();
+        this.watcherFront.on("target-available", this._onTargetAvailable);
+        this.watcherFront.on("target-destroyed", this._onTargetDestroyed);
       }
     }
 
@@ -312,18 +314,10 @@ class TargetCommand extends EventEmitter {
         // When we switch to a new top level target, we don't have to stop and restart
         // Watcher listener as it is independant from the top level target.
         // This isn't the case for some Legacy Listeners, which fetch targets from the top level target
-        if (onlyLegacy) {
-          continue;
+        if (!onlyLegacy) {
+          await this.watcherFront.watchTargets(type);
         }
-        if (!this._startedListeningToWatcher) {
-          this._startedListeningToWatcher = true;
-          this.watcherFront.on("target-available", this._onTargetAvailable);
-          this.watcherFront.on("target-destroyed", this._onTargetDestroyed);
-        }
-        await this.watcherFront.watchTargets(type);
-        continue;
-      }
-      if (this.legacyImplementation[type]) {
+      } else if (this.legacyImplementation[type]) {
         await this.legacyImplementation[type].listen();
       } else {
         throw new Error(`Unsupported target type '${type}'`);
@@ -355,9 +349,7 @@ class TargetCommand extends EventEmitter {
         if (!onlyLegacy) {
           this.watcherFront.unwatchTargets(type);
         }
-        continue;
-      }
-      if (this.legacyImplementation[type]) {
+      } else if (this.legacyImplementation[type]) {
         this.legacyImplementation[type].unlisten();
       } else {
         throw new Error(`Unsupported target type '${type}'`);
diff --git a/devtools/shared/commands/target/tests/browser_target_list_various_descriptors.js b/devtools/shared/commands/target/tests/browser_target_list_various_descriptors.js
index a9deef99bb0a..b2203381a785 100644
--- a/devtools/shared/commands/target/tests/browser_target_list_various_descriptors.js
+++ b/devtools/shared/commands/target/tests/browser_target_list_various_descriptors.js
@@ -6,6 +6,7 @@
 // Test the TargetCommand API with all possible descriptors
 
 const TEST_URL = "https://example.org/document-builder.sjs?html=org";
+const SECOND_TEST_URL = "https://example.com/document-builder.sjs?html=org";
 const CHROME_WORKER_URL = CHROME_URL_ROOT + "test_worker.js";
 
 add_task(async function() {
@@ -20,7 +21,8 @@ add_task(async function() {
   const client = await createLocalClient();
   const mainRoot = client.mainRoot;
 
-  await testTab(mainRoot);
+  await testLocalTab(mainRoot);
+  await testRemoteTab(mainRoot);
   await testParentProcess(mainRoot);
   await testContentProcess(mainRoot);
   await testWorker(mainRoot);
@@ -55,8 +57,8 @@ async function testParentProcess(rootFront) {
   await waitForAllTargetsToBeAttached(targetList);
 }
 
-async function testTab(rootFront) {
-  info("Test TargetCommand against tab descriptor");
+async function testLocalTab(rootFront) {
+  info("Test TargetCommand against local tab descriptor (via getTab({ tab }))");
 
   const tab = await addTab(TEST_URL);
   const descriptor = await rootFront.getTab({ tab });
@@ -82,6 +84,56 @@ async function testTab(rootFront) {
   BrowserTestUtils.removeTab(tab);
 }
 
+async function testRemoteTab(rootFront) {
+  info(
+    "Test TargetCommand against remote tab descriptor (via getTab({ outerWindowID }))"
+  );
+
+  const tab = await addTab(TEST_URL);
+  const descriptor = await rootFront.getTab({
+    outerWindowID: tab.linkedBrowser.outerWindowID,
+  });
+  const commands = await descriptor.getCommands();
+  const targetList = commands.targetCommand;
+  await targetList.startListening();
+
+  const targets = await targetList.getAllTargets(targetList.ALL_TYPES);
+  is(targets.length, 1, "Got a unique target");
+  const targetFront = targets[0];
+  is(
+    targetFront,
+    targetList.targetFront,
+    "TargetCommand top target is the same as the first target"
+  );
+  is(
+    targetFront.targetType,
+    targetList.TYPES.FRAME,
+    "the tab target is of frame type"
+  );
+  is(targetFront.isTopLevel, true, "This is flagged as top level");
+
+  const browser = tab.linkedBrowser;
+  const onLoaded = BrowserTestUtils.browserLoaded(browser);
+  await BrowserTestUtils.loadURI(browser, SECOND_TEST_URL);
+  await onLoaded;
+
+  if (isFissionEnabled()) {
+    info("With fission, cross process switching destroy everything");
+    ok(targetFront.isDestroyed(), "Top level target is destroyed");
+    ok(descriptor.isDestroyed(), "Descriptor is also destroyed");
+  } else {
+    is(
+      targetList.targetFront,
+      targetFront,
+      "Without fission, the top target stays the same"
+    );
+  }
+
+  targetList.destroy();
+
+  BrowserTestUtils.removeTab(tab);
+}
+
 async function testWebExtension(rootFront) {
   info("Test TargetCommand against webextension descriptor");