diff --git a/testing/firefox-ui/tests/puppeteer/test_software_update.py b/testing/firefox-ui/tests/puppeteer/test_software_update.py
index 5d2e8deb7afe..c69aff178a42 100644
--- a/testing/firefox-ui/tests/puppeteer/test_software_update.py
+++ b/testing/firefox-ui/tests/puppeteer/test_software_update.py
@@ -29,8 +29,7 @@ class TestSoftwareUpdate(PuppeteerMixin, MarionetteTestCase):
         self.assertTrue(self.software_update.ABI)
 
     def test_allowed(self):
-        # Updates are only allowed when run via the UpdateTestCase class
-        self.assertFalse(self.software_update.allowed)
+        self.assertTrue(self.software_update.allowed)
 
     def test_build_info(self):
         self.software_update.update_url = self.marionette.absolute_url(
diff --git a/testing/geckodriver/src/prefs.rs b/testing/geckodriver/src/prefs.rs
index 171ccb6cb334..8f5c849f8ae5 100644
--- a/testing/geckodriver/src/prefs.rs
+++ b/testing/geckodriver/src/prefs.rs
@@ -21,12 +21,14 @@ lazy_static! {
         ("app.update.checkInstallTime", Pref::new(false)),
 
         // Disable automatically upgrading Firefox
+        // Bug 1508726: "disabledForTesting" has no effect in Marionette yet.
+        // As such automatically downloading updates, and installing those
+        // needs to be prevented. Sadly "app.update.auto" will not be enough
+        // anymore, because Windows has changed in how it handles updates. But
+        // at least we can workaround the problem on other platforms.
         //
-        // Note: Possible update tests could reset or flip the value to allow
-        // updates to be downloaded and applied.
-        ("app.update.disabledForTesting", Pref::new(true)),
-        // !!! For backward compatibility up to Firefox 64. Only remove
-        // when this Firefox version is no longer supported by geckodriver !!!
+        // DISCLAIMER: Don't remove or change this line until bug 1508726 has
+        // been fixed.
         ("app.update.auto", Pref::new(false)),
 
         // Enable the dump function, which sends messages to the system
diff --git a/testing/marionette/client/marionette_driver/geckoinstance.py b/testing/marionette/client/marionette_driver/geckoinstance.py
index b359b711af30..958121b8e148 100644
--- a/testing/marionette/client/marionette_driver/geckoinstance.py
+++ b/testing/marionette/client/marionette_driver/geckoinstance.py
@@ -500,12 +500,14 @@ class DesktopInstance(GeckoInstance):
         "app.update.checkInstallTime": False,
 
         # Disable automatically upgrading Firefox
+        # Bug 1508726: "disabledForTesting" has no effect in Marionette yet.
+        # As such automatically downloading updates, and installing those
+        # needs to be prevented. Sadly "app.update.auto" will not be enough
+        # anymore, because Windows has changed in how it handles updates. But
+        # at least we can workaround the problem on other platforms.
         #
-        # Note: Possible update tests could reset or flip the value to allow
-        # updates to be downloaded and applied.
-        "app.update.disabledForTesting": True,
-        # !!! For backward compatibility up to Firefox 64. Only remove
-        # when this Firefox version is no longer supported by the client !!!
+        # DISCLAIMER: Don't remove or change this line until bug 1508726 has
+        # been fixed.
         "app.update.auto": False,
 
         # Don't show the content blocking introduction panel
diff --git a/testing/marionette/components/marionette.js b/testing/marionette/components/marionette.js
index ab4ff85ac2df..cd159ca4ff2e 100644
--- a/testing/marionette/components/marionette.js
+++ b/testing/marionette/components/marionette.js
@@ -64,13 +64,6 @@ const RECOMMENDED_PREFS = new Map([
   // Make sure Shield doesn't hit the network.
   ["app.normandy.api_url", ""],
 
-  // Disable automatically upgrading Firefox
-  //
-  // Note: This preference should have already been set by the client when
-  // creating the profile. But if not and to absolutely make sure that updates
-  // of Firefox aren't downloaded and applied, enforce its presence.
-  ["app.update.disabledForTesting", true],
-
   // Increase the APZ content response timeout in tests to 1 minute.
   // This is to accommodate the fact that test environments tends to be
   // slower than production environments (with the b2g emulator being
diff --git a/testing/marionette/harness/marionette_harness/tests/unit/test_marionette.py b/testing/marionette/harness/marionette_harness/tests/unit/test_marionette.py
index cdd4dc4c60b6..7837b0181ca4 100644
--- a/testing/marionette/harness/marionette_harness/tests/unit/test_marionette.py
+++ b/testing/marionette/harness/marionette_harness/tests/unit/test_marionette.py
@@ -61,17 +61,6 @@ class TestMarionette(MarionetteTestCase):
         self.assertEqual(current_socket_timeout,
                          self.marionette.client._sock.gettimeout())
 
-    def test_application_update_disabled(self):
-        # Updates of the application should always be disabled by default
-        with self.marionette.using_context("chrome"):
-            update_allowed = self.marionette.execute_script("""
-              let aus = Cc['@mozilla.org/updates/update-service;1']
-                        .getService(Ci.nsIApplicationUpdateService);
-              return aus.canCheckForUpdates;
-            """)
-
-        self.assertFalse(update_allowed)
-
 
 class TestContext(MarionetteTestCase):