diff --git a/browser/actors/PromptParent.jsm b/browser/actors/PromptParent.jsm
index 48b16329dc74..3cbd66072c71 100644
--- a/browser/actors/PromptParent.jsm
+++ b/browser/actors/PromptParent.jsm
@@ -270,6 +270,15 @@ class PromptParent extends JSWindowActorParent {
     let browsingContext = this.browsingContext.top;
 
     let browser = browsingContext.embedderElement;
+    let promptRequiresBrowser =
+      args.modalType === Services.prompt.MODAL_TYPE_TAB ||
+      args.modalType === Services.prompt.MODAL_TYPE_CONTENT;
+    if (promptRequiresBrowser && !browser) {
+      let modal_type =
+        args.modalType === Services.prompt.MODAL_TYPE_TAB ? "tab" : "content";
+      throw new Error(`Cannot ${modal_type}-prompt without a browser!`);
+    }
+
     let win;
 
     // If we are a chrome actor we can use the associated chrome win.
@@ -284,7 +293,7 @@ class PromptParent extends JSWindowActorParent {
     // passed window is the hidden window).
     // See bug 875157 comment 30 for more..
     if (win?.winUtils && !win.winUtils.isParentWindowMainWidgetVisible) {
-      throw new Error("Cannot call openModalWindow on a hidden window");
+      throw new Error("Cannot open a prompt in a hidden window");
     }
 
     try {
@@ -304,18 +313,7 @@ class PromptParent extends JSWindowActorParent {
       // Convert args object to a prop bag for the dialog to consume.
       let bag;
 
-      if (
-        (args.modalType === Services.prompt.MODAL_TYPE_TAB ||
-          args.modalType === Services.prompt.MODAL_TYPE_CONTENT) &&
-        win?.gBrowser?.getTabDialogBox
-      ) {
-        if (!browser) {
-          let modal_type =
-            args.modalType === Services.prompt.MODAL_TYPE_TAB
-              ? "tab"
-              : "content";
-          throw new Error(`Cannot ${modal_type}-prompt without a browser!`);
-        }
+      if (promptRequiresBrowser && win?.gBrowser?.getTabDialogBox) {
         // Tab or content level prompt
         let dialogBox = win.gBrowser.getTabDialogBox(browser);
 
diff --git a/browser/base/content/test/tabPrompts/browser.ini b/browser/base/content/test/tabPrompts/browser.ini
index 2388fe98982d..e0ac6d5c4965 100644
--- a/browser/base/content/test/tabPrompts/browser.ini
+++ b/browser/base/content/test/tabPrompts/browser.ini
@@ -9,5 +9,6 @@ support-files = file_beforeunload_stop.html
 [browser_openPromptInBackgroundTab.js]
 support-files = openPromptOffTimeout.html
 [browser_promptFocus.js]
+[browser_prompt_closed_window.js]
 [browser_switchTabPermissionPrompt.js]
 [browser_windowPrompt.js]
diff --git a/browser/base/content/test/tabPrompts/browser_prompt_closed_window.js b/browser/base/content/test/tabPrompts/browser_prompt_closed_window.js
new file mode 100644
index 000000000000..9b842bf57f0d
--- /dev/null
+++ b/browser/base/content/test/tabPrompts/browser_prompt_closed_window.js
@@ -0,0 +1,40 @@
+/* Any copyright is dedicated to the Public Domain.
+   http://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+/**
+ * Check that if we loop prompts from a closed tab, they don't
+ * start showing up as window prompts.
+ */
+add_task(async function test_closed_tab_doesnt_show_prompt() {
+  let newWin = await BrowserTestUtils.openNewBrowserWindow();
+
+  // Get a promise for the initial, in-tab prompt:
+  let promptPromise = BrowserTestUtils.promiseAlertDialogOpen();
+  await ContentTask.spawn(newWin.gBrowser.selectedBrowser, [], function() {
+    // Don't want to block, so use setTimeout with 0 timeout:
+    content.setTimeout(
+      () =>
+        content.eval(
+          'let i = 0; while (!prompt("Prompts a lot!") && i++ < 10);'
+        ),
+      0
+    );
+  });
+  // wait for the first prompt to have appeared:
+  await promptPromise;
+
+  // Now close the containing tab, and check for windowed prompts appearing.
+  let opened = false;
+  let obs = () => {
+    opened = true;
+  };
+  Services.obs.addObserver(obs, "domwindowopened");
+  registerCleanupFunction(() =>
+    Services.obs.removeObserver(obs, "domwindowopened")
+  );
+  await BrowserTestUtils.closeWindow(newWin);
+
+  ok(!opened, "Should not have opened a prompt when closing the main window.");
+});