diff --git a/browser/components/extensions/parent/ext-devtools-panels.js b/browser/components/extensions/parent/ext-devtools-panels.js
index c1e357f8379a7..0e46b8370863f 100644
--- a/browser/components/extensions/parent/ext-devtools-panels.js
+++ b/browser/components/extensions/parent/ext-devtools-panels.js
@@ -156,7 +156,7 @@ class ParentDevToolsPanel extends BaseDevToolsPanel {
       // panelLabel is used to set the aria-label attribute (See Bug 1570645).
       panelLabel: title,
       tooltip: `DevTools Panel added by "${extensionName}" add-on.`,
-      isToolSupported: toolbox => toolbox.target.isLocalTab,
+      isToolSupported: toolbox => toolbox.commands.descriptorFront.isLocalTab,
       build: (window, toolbox) => {
         if (toolbox !== this.toolbox) {
           throw new Error(
diff --git a/devtools/client/definitions.js b/devtools/client/definitions.js
index 504ca5b7dbb30..955f97630317e 100644
--- a/devtools/client/definitions.js
+++ b/devtools/client/definitions.js
@@ -280,7 +280,9 @@ Tools.performance = {
     // use the performance panel; about:debugging provides a "Profile performance" button
     // which can be used instead, without having the overhead of starting a remote toolbox.
     // Also accept the Browser Toolbox, so that we can profile its process via a second browser toolbox.
-    return toolbox.target.isLocalTab || toolbox.isBrowserToolbox;
+    return (
+      toolbox.commands.descriptorFront.isLocalTab || toolbox.isBrowserToolbox
+    );
   },
   build(frame, toolbox, commands) {
     return new NewPerformancePanel(frame, toolbox, commands);
@@ -490,7 +492,7 @@ exports.ToolboxButtons = [
       "toolbox.buttons.responsive",
       osString == "Darwin" ? "Cmd+Opt+M" : "Ctrl+Shift+M"
     ),
-    isToolSupported: toolbox => toolbox.target.isLocalTab,
+    isToolSupported: toolbox => toolbox.commands.descriptorFront.isLocalTab,
     onClick(event, toolbox) {
       const { localTab } = toolbox.commands.descriptorFront;
       const browserWindow = localTab.ownerDocument.defaultView;
diff --git a/devtools/client/framework/test/browser_commands_from_url.js b/devtools/client/framework/test/browser_commands_from_url.js
index c3a23f72803f1..aeeff7961bc25 100644
--- a/devtools/client/framework/test/browser_commands_from_url.js
+++ b/devtools/client/framework/test/browser_commands_from_url.js
@@ -21,7 +21,6 @@ SimpleTest.registerCleanupFunction(() => {
 
 function assertTarget(target, url, chrome = false) {
   is(target.url, url);
-  is(target.isLocalTab, false);
   is(target.chrome, chrome);
   is(target.isBrowsingContext, true);
 }
@@ -45,7 +44,18 @@ add_task(async function() {
   );
   // Descriptor's getTarget will only work if the TargetCommand watches for the first top target
   await commands.targetCommand.startListening();
+
+  // For now, we can't spawn a commands flagged as 'local tab' via URL query params
+  // The only way to has isLocalTab is to create the toolbox via showToolboxForTab
+  // and spawn the command via CommandsFactory.forTab.
+  is(
+    commands.descriptorFront.isLocalTab,
+    false,
+    "Even if we refer to a local tab, isLocalTab is false (for now)"
+  );
+
   target = await commands.descriptorFront.getTarget();
+
   assertTarget(target, TEST_URI);
   await commands.destroy();
 
diff --git a/devtools/client/framework/test/browser_target_events.js b/devtools/client/framework/test/browser_target_events.js
index 3681e93ff3511..77fc6047f23fc 100644
--- a/devtools/client/framework/test/browser_target_events.js
+++ b/devtools/client/framework/test/browser_target_events.js
@@ -16,11 +16,18 @@ add_task(async function() {
   gBrowser.selectedTab = BrowserTestUtils.addTab(gBrowser);
   await BrowserTestUtils.browserLoaded(gBrowser.selectedBrowser);
 
-  const target = await createAndAttachTargetForTab(gBrowser.selectedTab);
-  is(target.localTab, gBrowser.selectedTab, "Target linked to the right tab.");
+  const commands = await CommandsFactory.forTab(gBrowser.selectedTab);
+  is(
+    commands.descriptorFront.localTab,
+    gBrowser.selectedTab,
+    "Target linked to the right tab."
+  );
 
-  const willNavigate = once(target, "will-navigate");
-  const navigate = once(target, "navigate");
+  await commands.targetCommand.startListening();
+  const { targetFront } = commands.targetCommand;
+
+  const willNavigate = once(targetFront, "will-navigate");
+  const navigate = once(targetFront, "navigate");
   SpecialPowers.spawn(gBrowser.selectedBrowser, [], () => {
     content.location = "data:text/html,<meta charset='utf8'/>test navigation";
   });
@@ -29,8 +36,10 @@ add_task(async function() {
   await navigate;
   ok(true, "navigate event received");
 
-  const onTargetDestroyed = once(target, "target-destroyed");
+  const onTargetDestroyed = once(targetFront, "target-destroyed");
   gBrowser.removeCurrentTab();
   await onTargetDestroyed;
   ok(true, "target destroyed received");
+
+  await commands.destroy();
 });
diff --git a/devtools/client/framework/toolbox-options.js b/devtools/client/framework/toolbox-options.js
index 474edf5162960..c0991c46a140c 100644
--- a/devtools/client/framework/toolbox-options.js
+++ b/devtools/client/framework/toolbox-options.js
@@ -358,7 +358,8 @@ OptionsPanel.prototype = {
           visibilityswitch: pref,
 
           // Only local tabs are currently supported as targets.
-          isToolSupported: toolbox => toolbox.target.isLocalTab,
+          isToolSupported: toolbox =>
+            toolbox.commands.descriptorFront.isLocalTab,
         })
       );
     }
diff --git a/devtools/client/fronts/descriptors/tab.js b/devtools/client/fronts/descriptors/tab.js
index 0a1d9c254dc62..c3bbc066491fb 100644
--- a/devtools/client/fronts/descriptors/tab.js
+++ b/devtools/client/fronts/descriptors/tab.js
@@ -249,7 +249,6 @@ class TabDescriptorFront extends DescriptorMixin(
       this._targetFront.off("target-destroyed", this._onTargetDestroyed);
     }
     this._targetFront = targetFront;
-    targetFront.setDescriptor(this);
 
     targetFront.on("target-destroyed", this._onTargetDestroyed);
 
diff --git a/devtools/client/fronts/targets/target-mixin.js b/devtools/client/fronts/targets/target-mixin.js
index 8db2929e01497..57938cac58ec6 100644
--- a/devtools/client/fronts/targets/target-mixin.js
+++ b/devtools/client/fronts/targets/target-mixin.js
@@ -120,42 +120,6 @@ function TargetMixin(parentClass) {
       return true;
     }
 
-    /**
-     * Get the descriptor front for this target.
-     *
-     * TODO: Should be removed. This is misleading as only the top level target should have a descriptor.
-     * This will return null for targets created by the Watcher actor and will still be defined
-     * by targets created by RootActor methods (listSomething methods).
-     */
-    get descriptorFront() {
-      if (this.isDestroyed()) {
-        throw new Error("Descriptor already destroyed for target: " + this);
-      }
-
-      if (this.isWorkerTarget) {
-        return this;
-      }
-
-      if (this._descriptorFront) {
-        return this._descriptorFront;
-      }
-
-      if (this.parentFront.typeName.endsWith("Descriptor")) {
-        return this.parentFront;
-      }
-      throw new Error("Missing descriptor for target: " + this);
-    }
-
-    /**
-     * Top-level targets created on the server will not be created and managed
-     * by a descriptor front. Instead they are created by the Watcher actor.
-     * On the client side we manually re-establish a link between the descriptor
-     * and the new top-level target.
-     */
-    setDescriptor(descriptorFront) {
-      this._descriptorFront = descriptorFront;
-    }
-
     get targetType() {
       return this._targetType;
     }
@@ -272,24 +236,6 @@ function TargetMixin(parentClass) {
       return this.client.traits[traitName];
     }
 
-    get isLocalTab() {
-      // Worker Target is also the Descriptor,
-      // so avoid infinite loop.
-      if (this.isWorkerTarget) {
-        return false;
-      }
-      return !!this.descriptorFront?.isLocalTab;
-    }
-
-    get localTab() {
-      // Worker Target is also the Descriptor,
-      // so avoid infinite loop.
-      if (this.isWorkerTarget) {
-        return null;
-      }
-      return this.descriptorFront?.localTab || null;
-    }
-
     // Get a promise of the RootActor's form
     get root() {
       return this.client.mainRoot.rootForm;
diff --git a/devtools/client/inspector/test/browser_inspector_initialization.js b/devtools/client/inspector/test/browser_inspector_initialization.js
index 81c174a07fd0d..efbe88e44ee8a 100644
--- a/devtools/client/inspector/test/browser_inspector_initialization.js
+++ b/devtools/client/inspector/test/browser_inspector_initialization.js
@@ -38,7 +38,6 @@ async function testToolboxInitialization(tab) {
 
   ok(true, "Inspector started, and notification received.");
   ok(inspector, "Inspector instance is accessible.");
-  is(inspector.currentTarget.localTab, tab, "Valid target.");
 
   await selectNode("p", inspector);
   await testMarkupView("p", inspector);
diff --git a/devtools/client/inspector/test/browser_inspector_pseudoclass-lock.js b/devtools/client/inspector/test/browser_inspector_pseudoclass-lock.js
index fd5b25c30f462..d94230a984c24 100644
--- a/devtools/client/inspector/test/browser_inspector_pseudoclass-lock.js
+++ b/devtools/client/inspector/test/browser_inspector_pseudoclass-lock.js
@@ -20,9 +20,12 @@ const TEST_URL =
 
 add_task(async function() {
   info("Creating the test tab and opening the rule-view");
-  let { toolbox, inspector, highlighterTestFront } = await openInspectorForURL(
-    TEST_URL
-  );
+  let {
+    tab,
+    toolbox,
+    inspector,
+    highlighterTestFront,
+  } = await openInspectorForURL(TEST_URL);
 
   info("Selecting the ruleview sidebar");
   inspector.sidebar.select("ruleview");
@@ -80,7 +83,6 @@ add_task(async function() {
   );
 
   info("Destroying the toolbox");
-  const tab = toolbox.target.localTab;
   await toolbox.destroy();
 
   // As the toolbox get destroyed, we need to fetch a new test-actor
diff --git a/devtools/client/inspector/test/browser_inspector_reload_xul.js b/devtools/client/inspector/test/browser_inspector_reload_xul.js
index 5245797dd930f..013c0543aab8f 100644
--- a/devtools/client/inspector/test/browser_inspector_reload_xul.js
+++ b/devtools/client/inspector/test/browser_inspector_reload_xul.js
@@ -17,7 +17,6 @@ add_task(async function() {
 async function testToolboxInitialization(tab, inspector, toolbox) {
   ok(true, "Inspector started, and notification received.");
   ok(inspector, "Inspector instance is accessible.");
-  is(inspector.currentTarget.localTab, tab, "Valid target.");
 
   await selectNode("#p", inspector);
   await testMarkupView("#p", inspector);
diff --git a/devtools/client/netmonitor/test/head.js b/devtools/client/netmonitor/test/head.js
index a03bb617e837f..563bd617da7fb 100644
--- a/devtools/client/netmonitor/test/head.js
+++ b/devtools/client/netmonitor/test/head.js
@@ -363,7 +363,7 @@ function restartNetMonitor(monitor, { requestCount }) {
   info("Restarting the specified network monitor.");
 
   return (async function() {
-    const tab = monitor.toolbox.target.localTab;
+    const tab = monitor.commands.descriptorFront.localTab;
     const url = tab.linkedBrowser.currentURI.spec;
 
     await waitForAllNetworkUpdateEvents();
diff --git a/devtools/client/styleeditor/StyleEditorUI.sys.mjs b/devtools/client/styleeditor/StyleEditorUI.sys.mjs
index 3337e1e980f36..02dd6b7d6b212 100644
--- a/devtools/client/styleeditor/StyleEditorUI.sys.mjs
+++ b/devtools/client/styleeditor/StyleEditorUI.sys.mjs
@@ -1446,8 +1446,8 @@ export class StyleEditorUI extends EventEmitter {
    *         Object with width or/and height properties.
    */
   async #launchResponsiveMode(options = {}) {
-    const tab = this.currentTarget.localTab;
-    const win = this.currentTarget.localTab.ownerDocument.defaultView;
+    const tab = this.#commands.descriptorFront.localTab;
+    const win = tab.ownerDocument.defaultView;
 
     await lazy.ResponsiveUIManager.openIfNeeded(win, tab, {
       trigger: "style_editor",
diff --git a/devtools/client/webconsole/test/browser/browser_webconsole_multiple_windows_and_tabs.js b/devtools/client/webconsole/test/browser/browser_webconsole_multiple_windows_and_tabs.js
index 7048e4529e81f..ea7f332e51a18 100644
--- a/devtools/client/webconsole/test/browser/browser_webconsole_multiple_windows_and_tabs.js
+++ b/devtools/client/webconsole/test/browser/browser_webconsole_multiple_windows_and_tabs.js
@@ -37,7 +37,7 @@ add_task(async function() {
   for (const tab of tabs) {
     // Open the console in tab${i}.
     const hud = await openConsole(tab);
-    const browser = hud.currentTarget.localTab.linkedBrowser;
+    const browser = hud.commands.descriptorFront.localTab.linkedBrowser;
     const message = "message for tab " + tabs.indexOf(tab);
 
     // Log a message in the newly opened console.
diff --git a/devtools/docs/user/devtoolsapi/index.rst b/devtools/docs/user/devtoolsapi/index.rst
index 8d86db110d002..f1673e212873e 100644
--- a/devtools/docs/user/devtoolsapi/index.rst
+++ b/devtools/docs/user/devtoolsapi/index.rst
@@ -764,7 +764,7 @@ Register a tool
     },
 
     isToolSupported: function(toolbox) {
-      return toolbox.target.isLocalTab;
+      return toolbox.commands.descriptorFront.isLocalTab;
     },
 
     build: function(iframeWindow, toolbox, node) {
diff --git a/toolkit/components/extensions/ExtensionParent.jsm b/toolkit/components/extensions/ExtensionParent.jsm
index 98da1f3705499..3d174849873bb 100644
--- a/toolkit/components/extensions/ExtensionParent.jsm
+++ b/toolkit/components/extensions/ExtensionParent.jsm
@@ -881,9 +881,8 @@ class DevToolsExtensionPageContextParent extends ExtensionPageContextParent {
     for (const resource of resources) {
       const { targetFront } = resource;
       if (targetFront.isTopLevel && resource.name === "dom-complete") {
-        const url = targetFront.localTab.linkedBrowser.currentURI.spec;
         for (const listener of this._onNavigatedListeners) {
-          listener(url);
+          listener(targetFront.url);
         }
       }
     }