diff --git a/toolkit/components/backgroundtasks/tests/xpcshell/test_backgroundtask_locked_profile.js b/toolkit/components/backgroundtasks/tests/xpcshell/test_backgroundtask_locked_profile.js
new file mode 100644
index 000000000000..20583aa4200a
--- /dev/null
+++ b/toolkit/components/backgroundtasks/tests/xpcshell/test_backgroundtask_locked_profile.js
@@ -0,0 +1,42 @@
+/* -*- indent-tabs-mode: nil; js-indent-level: 2 -*-
+ * vim: sw=4 ts=4 sts=4 et
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this
+ * file, You can obtain one at http://mozilla.org/MPL/2.0/. */
+
+// Setup that allows to use the profile service, lifted from
+// `toolkit/profile/xpcshell/head.js`.
+let gProfD = do_get_profile();
+let gDataHome = gProfD.clone();
+gDataHome.append("data");
+gDataHome.createUnique(Ci.nsIFile.DIRECTORY_TYPE, 0o755);
+let gDataHomeLocal = gProfD.clone();
+gDataHomeLocal.append("local");
+gDataHomeLocal.createUnique(Ci.nsIFile.DIRECTORY_TYPE, 0o755);
+
+let xreDirProvider = Cc["@mozilla.org/xre/directory-provider;1"].getService(
+  Ci.nsIXREDirProvider
+);
+xreDirProvider.setUserDataDirectory(gDataHome, false);
+xreDirProvider.setUserDataDirectory(gDataHomeLocal, true);
+
+add_task(async function test_backgroundtask_locked_profile() {
+  let profileService = Cc["@mozilla.org/toolkit/profile-service;1"].getService(
+    Ci.nsIToolkitProfileService
+  );
+
+  let profile = profileService.createUniqueProfile(
+    do_get_profile(),
+    "test_locked_profile"
+  );
+  let lock = profile.lock({});
+
+  try {
+    let exitCode = await do_backgroundtask("success", {
+      extraEnv: { XRE_PROFILE_PATH: lock.directory.path },
+    });
+    Assert.equal(1, exitCode);
+  } finally {
+    lock.unlock();
+  }
+});
diff --git a/toolkit/components/backgroundtasks/tests/xpcshell/xpcshell.ini b/toolkit/components/backgroundtasks/tests/xpcshell/xpcshell.ini
index 21d1dfefc388..b9c8205e43ba 100644
--- a/toolkit/components/backgroundtasks/tests/xpcshell/xpcshell.ini
+++ b/toolkit/components/backgroundtasks/tests/xpcshell/xpcshell.ini
@@ -10,6 +10,7 @@ support-files =
   CatBackgroundTaskRegistrationComponents.manifest
 
 [test_backgroundtask_exitcodes.js]
+[test_backgroundtask_locked_profile.js]
 [test_backgroundtask_policies.js]
 [test_backgroundtask_specific_pref.js]
 [test_backgroundtask_update_sync_manager.js]
diff --git a/toolkit/xre/nsAppRunner.cpp b/toolkit/xre/nsAppRunner.cpp
index eb95dd483f6c..a29f88892d6f 100644
--- a/toolkit/xre/nsAppRunner.cpp
+++ b/toolkit/xre/nsAppRunner.cpp
@@ -2289,6 +2289,14 @@ class ReturnAbortOnError {
     if (NS_SUCCEEDED(aRv) || aRv == NS_ERROR_LAUNCHED_CHILD_PROCESS) {
       return aRv;
     }
+#ifdef MOZ_BACKGROUNDTASKS
+    // A background task that fails to lock its profile will return
+    // NS_ERROR_UNEXPECTED and this will allow the task to exit with a
+    // non-zero exit code.
+    if (aRv == NS_ERROR_UNEXPECTED && BackgroundTasks::IsBackgroundTaskMode()) {
+      return aRv;
+    }
+#endif
     return NS_ERROR_ABORT;
   }
 
@@ -2400,6 +2408,14 @@ static ReturnAbortOnError ProfileLockedDialog(nsIFile* aProfileDir,
     rv = sb->FormatStringFromName("restartTitle", params, killTitle);
     NS_ENSURE_SUCCESS(rv, NS_ERROR_FAILURE);
 
+#ifdef MOZ_BACKGROUNDTASKS
+    if (BackgroundTasks::IsBackgroundTaskMode()) {
+      // This error is handled specially to exit with a non-zero exit code.
+      printf_stderr("%s\n", NS_LossyConvertUTF16toASCII(killMessage).get());
+      return NS_ERROR_UNEXPECTED;
+    }
+#endif
+
     if (gfxPlatform::IsHeadless()) {
       // TODO: make a way to turn off all dialogs when headless.
       Output(true, "%s\n", NS_LossyConvertUTF16toASCII(killMessage).get());
@@ -4496,14 +4512,17 @@ int XREMain::XRE_mainStartup(bool* aExitFlag) {
 
 #ifdef MOZ_BACKGROUNDTASKS
   if (BackgroundTasks::IsBackgroundTaskMode()) {
-    nsCOMPtr<nsIFile> file;
-    nsresult rv = BackgroundTasks::GetOrCreateTemporaryProfileDirectory(
-        getter_AddRefs(file));
-    if (NS_WARN_IF(NS_FAILED(rv))) {
-      return 1;
-    }
+    if (!EnvHasValue("XRE_PROFILE_PATH")) {
+      // Allow tests to specify profile path via the environment.
+      nsCOMPtr<nsIFile> file;
+      nsresult rv = BackgroundTasks::GetOrCreateTemporaryProfileDirectory(
+          getter_AddRefs(file));
+      if (NS_WARN_IF(NS_FAILED(rv))) {
+        return 1;
+      }
 
-    SaveFileToEnv("XRE_PROFILE_PATH", file);
+      SaveFileToEnv("XRE_PROFILE_PATH", file);
+    }
   }
 #endif