diff --git a/hermes_cli/gateway.py b/hermes_cli/gateway.py
index ab743b281f19..d40a9597028c 100644
--- a/hermes_cli/gateway.py
+++ b/hermes_cli/gateway.py
@@ -938,6 +938,32 @@ def _read_systemd_unit_environment(system: bool = False) -> dict[str, str]:
     return parsed
 
 
+def _hermes_home_from_systemd_unit_file(system: bool = False) -> str | None:
+    """Read ``HERMES_HOME`` from the on-disk unit file (not ``systemctl show``).
+
+    Prefer the file when refreshing/comparing: under ``sudo``, ``systemctl``
+    may be slow/unavailable in tests, and the on-disk unit is what
+    ``systemd_unit_is_current`` / ``refresh_systemd_unit_if_needed`` already
+    compare against.
+    """
+    unit_path = get_systemd_unit_path(system=system)
+    if not unit_path.exists():
+        return None
+    try:
+        text = unit_path.read_text(encoding="utf-8")
+    except OSError:
+        return None
+    for line in text.splitlines():
+        stripped = line.strip()
+        if not stripped.startswith("Environment="):
+            continue
+        body = stripped[len("Environment=") :].strip().strip('"')
+        if body.startswith("HERMES_HOME="):
+            value = body.split("=", 1)[1].strip().strip('"')
+            return value or None
+    return None
+
+
 def _sync_hermes_home_from_systemd_unit(system: bool) -> None:
     """When acting on a system-scope unit, adopt its ``HERMES_HOME``.
 
@@ -949,8 +975,11 @@ def _sync_hermes_home_from_systemd_unit(system: bool) -> None:
     """
     if not system:
         return
-    env = _read_systemd_unit_environment(system=True)
-    unit_home = env.get("HERMES_HOME", "").strip()
+    # Prefer the on-disk unit (source of truth for refresh/compare). Fall
+    # back to ``systemctl show`` for units that only exist in the manager.
+    unit_home = (_hermes_home_from_systemd_unit_file(system=True) or "").strip()
+    if not unit_home:
+        unit_home = _read_systemd_unit_environment(system=True).get("HERMES_HOME", "").strip()
     if not unit_home:
         return
     current = os.environ.get("HERMES_HOME", "").strip()
@@ -2830,6 +2859,13 @@ def systemd_unit_is_current(system: bool = False) -> bool:
     if not unit_path.exists():
         return False
 
+    # Under ``sudo hermes gateway … --system``, HERMES_HOME is often stripped
+    # and falls back to ``/root/.hermes``. Adopt the unit's pinned home first
+    # so TimeoutStopSec / WorkingDirectory / HERMES_HOME comparisons use the
+    # real operator config — otherwise start/restart "refresh" rewrites a
+    # correct unit from root's defaults and ``status`` keeps warning forever.
+    _sync_hermes_home_from_systemd_unit(system=system)
+
     installed = unit_path.read_text(encoding="utf-8")
     expected_user = _read_systemd_user_from_unit(unit_path) if system else None
     expected = generate_systemd_unit(system=system, run_as_user=expected_user)
@@ -2907,7 +2943,15 @@ def _refuse_temp_home_service_write(definition: str, kind: str) -> bool:
 def refresh_systemd_unit_if_needed(system: bool = False) -> bool:
     """Rewrite the installed systemd unit when the generated definition has changed."""
     unit_path = get_systemd_unit_path(system=system)
-    if not unit_path.exists() or systemd_unit_is_current(system=system):
+    if not unit_path.exists():
+        return False
+
+    # Sync before the current-check / regenerate path so a ``sudo`` shell
+    # does not bake root's config into a system unit that already pins the
+    # operator's HERMES_HOME. ``systemd_unit_is_current`` also syncs; doing
+    # it here keeps the write path safe even if that helper changes.
+    _sync_hermes_home_from_systemd_unit(system=system)
+    if systemd_unit_is_current(system=system):
         return False
 
     expected_user = _read_systemd_user_from_unit(unit_path) if system else None
@@ -3094,6 +3138,12 @@ def systemd_install(
     unit_path = get_systemd_unit_path(system=system)
     scope_flag = " --system" if system else ""
 
+    # Existing system units already pin HERMES_HOME; adopt it before any
+    # current-check / regenerate so ``sudo hermes gateway install --system``
+    # cannot "repair" a correct unit from root's config.
+    if unit_path.exists():
+        _sync_hermes_home_from_systemd_unit(system=system)
+
     if unit_path.exists() and not force:
         if not systemd_unit_is_current(system=system):
             print(
@@ -3184,6 +3234,9 @@ def systemd_start(system: bool = False):
         # Raises UserSystemdUnavailableError with a remediation message.
         _preflight_user_systemd()
     _require_service_installed("start", system=system)
+    # Adopt the unit's HERMES_HOME before refresh so sudo system starts do not
+    # rewrite TimeoutStopSec / env from /root/.hermes.
+    _sync_hermes_home_from_systemd_unit(system=system)
     refresh_systemd_unit_if_needed(system=system)
     _run_systemctl(["start", get_service_name()], system=system, check=True, timeout=30)
     print(f"✓ {_service_scope_label(system).capitalize()} service started")
@@ -3224,8 +3277,11 @@ def systemd_restart(system: bool = False):
     else:
         _preflight_user_systemd()
     _require_service_installed("restart", system=system)
-    refresh_systemd_unit_if_needed(system=system)
+    # Sync BEFORE refresh. Under sudo, refreshing first used to regenerate the
+    # unit from /root/.hermes (wrong drain timeout / env), then sync for PID
+    # lookup — leaving ``status`` stuck on "service definition is outdated".
     _sync_hermes_home_from_systemd_unit(system=system)
+    refresh_systemd_unit_if_needed(system=system)
     from gateway.status import get_running_pid
 
     pid = get_running_pid() or _systemd_main_pid(system=system)