diff --git a/qubesadmin/tests/vm/actions.py b/qubesadmin/tests/vm/actions.py
index 570bd87b5..eff775f2e 100644
--- a/qubesadmin/tests/vm/actions.py
+++ b/qubesadmin/tests/vm/actions.py
@@ -93,6 +93,51 @@ def test_011_run_windows(self):
             ('test-vm', 'qubes.VMShell', b'some command& exit\n'),
         ])
 
+    def test_012_run_linux_root(self):
+        self.app.expected_calls[
+            ("test-vm", "admin.vm.feature.CheckWithTemplate", "os", None)
+        ] = b"2\x00QubesFeatureNotFoundError\x00\x00Feature 'os' not set\x00"
+        self.app.expected_calls[
+            (
+                "test-vm",
+                "admin.vm.feature.CheckWithTemplate",
+                "supported-rpc.qubes.VMRootExec",
+                None,
+            )
+        ] = (
+            b"2\x00QubesFeatureNotFoundError\x00\x00"
+            b"Feature 'supported-rpc.qubes.VMRootExec' not set\x00"
+        )
+        self.vm.run("some command", user="root")
+        self.assertEqual(
+            self.app.service_calls,
+            [
+                ("test-vm", "qubes.VMShell", {"user": "root"}),
+                ("test-vm", "qubes.VMShell", b"some command; exit\n"),
+            ],
+        )
+
+    def test_013_run_linux_root_vmrootshell(self):
+        self.app.expected_calls[
+            ("test-vm", "admin.vm.feature.CheckWithTemplate", "os", None)
+        ] = b"2\x00QubesFeatureNotFoundError\x00\x00Feature 'os' not set\x00"
+        self.app.expected_calls[
+            (
+                "test-vm",
+                "admin.vm.feature.CheckWithTemplate",
+                "supported-rpc.qubes.VMRootExec",
+                None,
+            )
+        ] = b"0\x001"
+        self.vm.run("some command", user="root")
+        self.assertEqual(
+            self.app.service_calls,
+            [
+                ("test-vm", "qubes.VMRootShell", {}),
+                ("test-vm", "qubes.VMRootShell", b"some command; exit\n"),
+            ],
+        )
+
     def test_015_run_with_args_shell(self):
         self.app.expected_calls[
             ('test-vm', 'admin.vm.feature.CheckWithTemplate', 'vmexec',
diff --git a/qubesadmin/vm/__init__.py b/qubesadmin/vm/__init__.py
index 5ac7f1adb..55943747e 100644
--- a/qubesadmin/vm/__init__.py
+++ b/qubesadmin/vm/__init__.py
@@ -364,13 +364,20 @@ def run(self, command, input=None, **kwargs):
         # pylint: disable=redefined-builtin
         try:
             service = "qubes.VMShell"
-            if kwargs.get("user", None) == "root":
+            # intentionally check for qubes.VMRootExec, as this is when
+            # qubes.VMRootShell got force-user='root' in its config
+            if kwargs.get(
+                "user", None
+            ) == "root" and self.features.check_with_template(
+                "supported-rpc.qubes.VMRootExec", False
+            ):
+
                 kwargs.pop("user")
                 service = "qubes.VMRootShell"
             return self.run_service_for_stdio(
                 service,
                 input=self.prepare_input_for_vmshell(command, input),
-                **kwargs
+                **kwargs,
             )
         except subprocess.CalledProcessError as e:
             e.cmd = command