diff --git a/hermes_cli/gateway.py b/hermes_cli/gateway.py
index f29c42358a2e5..1852afbd8b8f5 100644
--- a/hermes_cli/gateway.py
+++ b/hermes_cli/gateway.py
@@ -2749,7 +2749,9 @@ def _systemd_watchdog_service_fields(
     return "notify", f"NotifyAccess=main\nWatchdogSec={seconds}s\n"
 
 
-def _append_node_dir_for_service(path_entries: list[str]) -> None:
+def _append_node_dir_for_service(
+    path_entries: list[str], hermes_root: Path | None = None
+) -> None:
     """Add the Node directory a generated service unit should use to *path_entries*.
 
     The Hermes-managed Node under ``$HERMES_HOME/node`` goes first when it
@@ -2757,16 +2759,27 @@ def _append_node_dir_for_service(path_entries: list[str]) -> None:
     a service unit is written once and then survives reboots, so resolving a
     system Node that happens to be ahead on the installing shell's PATH bakes
     the wrong interpreter in permanently — the exact failure the desktop
-    backend spawn was fixed for. Managed dirs are profile-scoped
-    (``get_hermes_home()``), so each profile's unit still names its own Node.
+    backend spawn was fixed for. Managed dirs are profile-scoped, so each
+    profile's unit still names its own Node.
+
+    *hermes_root* is the Hermes home the unit will run against. System units
+    installed via sudo MUST pass the **target user's** home: probing the
+    default (the calling user's — root's — tree) would bake root's Node into
+    the target user's unit. The probe swallows OSError: an unreadable
+    candidate dir (hardened home) means "skip the rung", not "crash the
+    generator".
 
     PATH lookup remains the fallback rung for installs with no managed Node.
     """
     from hermes_constants import iter_hermes_node_dirs
 
-    for directory in iter_hermes_node_dirs():
+    for directory in iter_hermes_node_dirs(hermes_root):
         entry = str(directory)
-        if directory.is_dir() and entry not in path_entries:
+        try:
+            present = directory.is_dir()
+        except OSError:
+            present = False
+        if present and entry not in path_entries:
             path_entries.append(entry)
 
     resolved_node = shutil.which("node")
@@ -2793,7 +2806,11 @@ def generate_systemd_unit(system: bool = False, run_as_user: str | None = None)
     venv_dir = str(detected_venv) if detected_venv else str(PROJECT_ROOT / "venv")
 
     path_entries = _build_service_path_dirs()
-    _append_node_dir_for_service(path_entries)
+    if not system:
+        # System units append the managed Node dirs later, once the TARGET
+        # user's Hermes home is known — probing here would stat the calling
+        # (sudo → root's) tree and bake the wrong user's Node into the unit.
+        _append_node_dir_for_service(path_entries)
 
     common_bin_paths = [
         "/usr/local/sbin",
@@ -2827,6 +2844,17 @@ def generate_systemd_unit(system: bool = False, run_as_user: str | None = None)
         working_dir = str(hermes_home) if hermes_home else _remap_path_for_user(working_dir, home_dir)
         venv_dir = _remap_path_for_user(venv_dir, home_dir)
         path_entries = [_remap_path_for_user(p, home_dir) for p in path_entries]
+        # Managed Node for the TARGET user's tree (see the skip above): probe
+        # the remapped hermes_home, not the calling user's. Prepend — the
+        # managed Node must outrank remapped shell-PATH entries, matching the
+        # user-unit ordering where it's appended before PATH capture.
+        _target_node_entries: list[str] = []
+        _append_node_dir_for_service(
+            _target_node_entries, Path(hermes_home) if hermes_home else None
+        )
+        path_entries = [
+            e for e in _target_node_entries if e not in path_entries
+        ] + path_entries
         path_entries.extend(_build_user_local_paths(Path(home_dir), path_entries))
         path_entries.extend(_build_wsl_interop_paths(path_entries))
         path_entries.extend(common_bin_paths)