diff --git a/hermes_cli/gateway.py b/hermes_cli/gateway.py
index b19ceaac9..1ca487364 100644
--- a/hermes_cli/gateway.py
+++ b/hermes_cli/gateway.py
@@ -618,6 +618,24 @@ def _build_user_local_paths(home: Path, path_entries: list[str]) -> list[str]:
     return [p for p in candidates if p not in path_entries and Path(p).exists()]
 
 
+def _remap_path_for_user(path: str, target_home_dir: str) -> str:
+    """Remap *path* from the current user's home to *target_home_dir*.
+
+    If *path* lives under ``Path.home()`` the corresponding prefix is swapped
+    to *target_home_dir*; otherwise the path is returned unchanged.
+
+      /root/.hermes/hermes-agent  -> /home/alice/.hermes/hermes-agent
+      /opt/hermes                 -> /opt/hermes  (kept as-is)
+    """
+    current_home = Path.home().resolve()
+    resolved = Path(path).resolve()
+    try:
+        relative = resolved.relative_to(current_home)
+        return str(Path(target_home_dir) / relative)
+    except ValueError:
+        return str(resolved)
+
+
 def _hermes_home_for_target_user(target_home_dir: str) -> str:
     """Remap the current HERMES_HOME to the equivalent under a target user's home.
 
@@ -665,6 +683,15 @@ def generate_systemd_unit(system: bool = False, run_as_user: str | None = None)
         username, group_name, home_dir = _system_service_identity(run_as_user)
         hermes_home = _hermes_home_for_target_user(home_dir)
         profile_arg = _profile_arg(hermes_home)
+        # Remap all paths that may resolve under the calling user's home
+        # (e.g. /root/) to the target user's home so the service can
+        # actually access them.
+        python_path = _remap_path_for_user(python_path, home_dir)
+        working_dir = _remap_path_for_user(working_dir, home_dir)
+        venv_dir = _remap_path_for_user(venv_dir, home_dir)
+        venv_bin = _remap_path_for_user(venv_bin, home_dir)
+        node_bin = _remap_path_for_user(node_bin, home_dir)
+        path_entries = [_remap_path_for_user(p, home_dir) for p in path_entries]
         path_entries.extend(_build_user_local_paths(Path(home_dir), path_entries))
         path_entries.extend(common_bin_paths)
         sane_path = ":".join(path_entries)
diff --git a/tests/hermes_cli/test_gateway_service.py b/tests/hermes_cli/test_gateway_service.py
index aa21793ae..23ad21b36 100644
--- a/tests/hermes_cli/test_gateway_service.py
+++ b/tests/hermes_cli/test_gateway_service.py
@@ -754,3 +754,63 @@ class TestProfileArg:
         plist = gateway_cli.generate_launchd_plist()
         assert "<string>--profile</string>" in plist
         assert "<string>mybot</string>" in plist
+
+
+class TestRemapPathForUser:
+    """Unit tests for _remap_path_for_user()."""
+
+    def test_remaps_path_under_current_home(self, monkeypatch, tmp_path):
+        monkeypatch.setattr(Path, "home", lambda: tmp_path / "root")
+        (tmp_path / "root").mkdir()
+        result = gateway_cli._remap_path_for_user(
+            str(tmp_path / "root" / ".hermes" / "hermes-agent"),
+            str(tmp_path / "alice"),
+        )
+        assert result == str(tmp_path / "alice" / ".hermes" / "hermes-agent")
+
+    def test_keeps_system_path_unchanged(self, monkeypatch, tmp_path):
+        monkeypatch.setattr(Path, "home", lambda: tmp_path / "root")
+        (tmp_path / "root").mkdir()
+        result = gateway_cli._remap_path_for_user("/opt/hermes", str(tmp_path / "alice"))
+        assert result == "/opt/hermes"
+
+    def test_noop_when_same_user(self, monkeypatch, tmp_path):
+        monkeypatch.setattr(Path, "home", lambda: tmp_path / "alice")
+        (tmp_path / "alice").mkdir()
+        original = str(tmp_path / "alice" / ".hermes" / "hermes-agent")
+        result = gateway_cli._remap_path_for_user(original, str(tmp_path / "alice"))
+        assert result == original
+
+
+class TestSystemUnitPathRemapping:
+    """System units must remap ALL paths from the caller's home to the target user."""
+
+    def test_system_unit_has_no_root_paths(self, monkeypatch, tmp_path):
+        root_home = tmp_path / "root"
+        root_home.mkdir()
+        project = root_home / ".hermes" / "hermes-agent"
+        project.mkdir(parents=True)
+        venv_bin = project / "venv" / "bin"
+        venv_bin.mkdir(parents=True)
+        (venv_bin / "python").write_text("")
+
+        target_home = "/home/alice"
+
+        monkeypatch.setattr(Path, "home", lambda: root_home)
+        monkeypatch.setenv("HERMES_HOME", str(root_home / ".hermes"))
+        monkeypatch.setattr(gateway_cli, "get_hermes_home", lambda: root_home / ".hermes")
+        monkeypatch.setattr(gateway_cli, "PROJECT_ROOT", project)
+        monkeypatch.setattr(gateway_cli, "_detect_venv_dir", lambda: project / "venv")
+        monkeypatch.setattr(gateway_cli, "get_python_path", lambda: str(venv_bin / "python"))
+        monkeypatch.setattr(
+            gateway_cli, "_system_service_identity",
+            lambda run_as_user=None: ("alice", "alice", target_home),
+        )
+
+        unit = gateway_cli.generate_systemd_unit(system=True)
+
+        # No root paths should leak into the unit
+        assert str(root_home) not in unit
+        # Target user paths should be present
+        assert "/home/alice" in unit
+        assert "WorkingDirectory=/home/alice/.hermes/hermes-agent" in unit