diff --git a/modules/libpref/init/all.js b/modules/libpref/init/all.js
index 9bed94bc4b51..62d50869dd3f 100644
--- a/modules/libpref/init/all.js
+++ b/modules/libpref/init/all.js
@@ -4411,6 +4411,14 @@ pref("browser.sanitizer.loglevel", "Warn");
 // To disable blocking of auth prompts, set the limit to -1.
 pref("prompts.authentication_dialog_abuse_limit", 2);
 
+// The prompt type to use for http auth prompts
+// content: 1, tab: 2, window: 3
+#ifdef NIGHTLY_BUILD
+  pref("prompts.modalType.httpAuth", 2);
+#else
+  pref("prompts.modalType.httpAuth", 3);
+#endif
+
 // Payment Request API preferences
 pref("dom.payments.loglevel", "Warn");
 pref("dom.payments.defaults.saveCreditCard", false);
diff --git a/toolkit/components/passwordmgr/LoginManagerAuthPrompter.jsm b/toolkit/components/passwordmgr/LoginManagerAuthPrompter.jsm
index 9ef00ad4e6dc..e048438909d3 100644
--- a/toolkit/components/passwordmgr/LoginManagerAuthPrompter.jsm
+++ b/toolkit/components/passwordmgr/LoginManagerAuthPrompter.jsm
@@ -756,14 +756,29 @@ LoginManagerAuthPrompter.prototype = {
           this._browser
         );
       }
-      ok = Services.prompt.promptAuth(
-        this._chromeWindow,
-        aChannel,
-        aLevel,
-        aAuthInfo,
-        checkboxLabel,
-        checkbox
-      );
+      if (this._browser) {
+        ok = Services.prompt.promptAuthBC(
+          this._browser.browsingContext,
+          LoginManagerAuthPrompter.promptAuthModalType,
+          aChannel,
+          aLevel,
+          aAuthInfo,
+          checkboxLabel,
+          checkbox
+        );
+      } else {
+        // Can't tab prompt without browser. Fallback to window prompt.
+        // For cases where this._chromeWindow is defined, this will keep our
+        // parent relationship intact as opposed to passing null above.
+        ok = Services.prompt.promptAuth(
+          this._chromeWindow,
+          aChannel,
+          aLevel,
+          aAuthInfo,
+          checkboxLabel,
+          checkbox
+        );
+      }
     }
 
     let [username, password] = this._GetAuthInfo(aAuthInfo);
@@ -1296,6 +1311,13 @@ XPCOMUtils.defineLazyGetter(LoginManagerAuthPrompter.prototype, "log", () => {
   return logger.log.bind(logger);
 });
 
+XPCOMUtils.defineLazyPreferenceGetter(
+  LoginManagerAuthPrompter,
+  "promptAuthModalType",
+  "prompts.modalType.httpAuth",
+  Services.prompt.MODAL_TYPE_WINDOW
+);
+
 const EXPORTED_SYMBOLS = [
   "LoginManagerAuthPromptFactory",
   "LoginManagerAuthPrompter",