diff --git a/browser/components/genai/GenAI.sys.mjs b/browser/components/genai/GenAI.sys.mjs
index ab4b461aab5..2cd404595e7 100644
--- a/browser/components/genai/GenAI.sys.mjs
+++ b/browser/components/genai/GenAI.sys.mjs
@@ -435,6 +435,8 @@ export const GenAI = {
     // Hide shortcuts and panel
     const hide = () => {
       aiActionButton.setAttribute("type", buttonDefaultState);
+      aiActionButton.removeEventListener("mouseover", aiActionButton.listener);
+      aiActionButton.listener = null;
       chatShortcutsOptionsPanel.hidePopup();
       selectionShortcutActionPanel.hidePopup();
     };
@@ -486,7 +488,7 @@ export const GenAI = {
         aiActionButton.setAttribute("type", buttonDefaultState);
 
         // Detect hover to build and open the popup
-        aiActionButton.addEventListener("mouseover", async () => {
+        aiActionButton.listener = async () => {
           if (aiActionButton.hasAttribute("active")) {
             return;
           }
@@ -592,7 +594,8 @@ export const GenAI = {
             provider: this.getProviderId(),
             warning: showWarning,
           });
-        });
+        };
+        aiActionButton.addEventListener("mouseover", aiActionButton.listener);
 
         // Save the latest selection so it can be used by popup
         aiActionButton.data = data;
diff --git a/browser/components/genai/tests/browser/browser_chat_shortcuts.js b/browser/components/genai/tests/browser/browser_chat_shortcuts.js
index eb7f6028685..0fb240bc56d 100644
--- a/browser/components/genai/tests/browser/browser_chat_shortcuts.js
+++ b/browser/components/genai/tests/browser/browser_chat_shortcuts.js
@@ -107,6 +107,44 @@ add_task(async function test_show_shortcuts() {
   });
 });
 
+/**
+ * Check that shortcuts shown on second tab
+ */
+add_task(async function test_show_shortcuts_second_tab() {
+  // NB: this test runs after test_show_shortcuts, which showed shortcuts
+  await BrowserTestUtils.withNewTab(
+    "data:text/html,<title>second</title>page",
+    async browser => {
+      await SimpleTest.promiseFocus(browser);
+      const selectPromise = SpecialPowers.spawn(browser, [], () => {
+        ContentTaskUtils.waitForCondition(() => content.getSelection());
+      });
+      goDoCommand("cmd_selectAll");
+      await selectPromise;
+      BrowserTestUtils.synthesizeMouseAtCenter(
+        browser,
+        { type: "mouseup" },
+        browser
+      );
+
+      await TestUtils.waitForCondition(() => {
+        const panelElement = document.getElementById(
+          "selection-shortcut-action-panel"
+        );
+        return panelElement.getAttribute("panelopen") === "true";
+      });
+      const sandbox = sinon.createSandbox();
+      const stub = sandbox.stub(GenAI, "addAskChatItems");
+
+      const shortcuts = document.querySelector("#ai-action-button");
+      EventUtils.sendMouseEvent({ type: "mouseover" }, shortcuts);
+
+      Assert.equal(stub.callCount, 1, "Shortcuts added on select");
+      Assert.equal(stub.firstCall.args[0], browser, "Got correct browser");
+    }
+  );
+});
+
 /**
  * Check that the warning label is shown when too much text is selected
  */

diff --git a/browser/components/genai/tests/browser/browser_chat_shortcuts.js b/browser/components/genai/tests/browser/browser_chat_shortcuts.js
index eb7f6028685..0fb240bc56d 100644
--- a/browser/components/genai/tests/browser/browser_chat_shortcuts.js
+++ b/browser/components/genai/tests/browser/browser_chat_shortcuts.js
@@ -107,6 +107,44 @@ add_task(async function test_show_shortcuts() {
   });
 });
 
+/**
+ * Check that shortcuts shown on second tab
+ */
+add_task(async function test_show_shortcuts_second_tab() {
+  // NB: this test runs after test_show_shortcuts, which showed shortcuts
+  await BrowserTestUtils.withNewTab(
+    "data:text/html,<title>second</title>page",
+    async browser => {
+      await SimpleTest.promiseFocus(browser);
+      const selectPromise = SpecialPowers.spawn(browser, [], () => {
+        ContentTaskUtils.waitForCondition(() => content.getSelection());
+      });
+      goDoCommand("cmd_selectAll");
+      await selectPromise;
+      BrowserTestUtils.synthesizeMouseAtCenter(
+        browser,
+        { type: "mouseup" },
+        browser
+      );
+
+      await TestUtils.waitForCondition(() => {
+        const panelElement = document.getElementById(
+          "selection-shortcut-action-panel"
+        );
+        return panelElement.getAttribute("panelopen") === "true";
+      });
+      const sandbox = sinon.createSandbox();
+      const stub = sandbox.stub(GenAI, "addAskChatItems");
+
+      const shortcuts = document.querySelector("#ai-action-button");
+      EventUtils.sendMouseEvent({ type: "mouseover" }, shortcuts);
+
+      Assert.equal(stub.callCount, 1, "Shortcuts added on select");
+      Assert.equal(stub.firstCall.args[0], browser, "Got correct browser");
+    }
+  );
+});
+
 /**
  * Check that the warning label is shown when too much text is selected
  */