diff --git a/hermes_cli/container_boot.py b/hermes_cli/container_boot.py
index 3d99681a715..fc85529bbce 100644
--- a/hermes_cli/container_boot.py
+++ b/hermes_cli/container_boot.py
@@ -38,6 +38,29 @@ log = logging.getLogger(__name__)
 # durable start/stop intent across pod/container recreation.
 _AUTOSTART_STATES = frozenset({"running"})
 
+# Transient runtime sub-states of a RUNNING gateway. A gateway only ever
+# reaches these while it is up and serving — `draining` is written by the
+# drain watcher / scale-to-zero go-dormant path when an in-flight quiesce
+# begins (gateway/run.py). It is NOT an operator stop and NOT a failed boot.
+#
+# When a gateway is hard-killed *while draining* (a container/VM recreate
+# SIGTERMs it before `_stop_impl` reaches its terminal-state persist), the
+# last value left in gateway_state.json is `draining`. With no explicit
+# `desired_state` to fall back to, treating that literal value as the
+# autostart intent would leave the gateway DOWN on every subsequent boot —
+# the gateway never comes back, the dashboard is up but messaging stays dark
+# (observed on a relay-opted-in staging instance, 2026-06). Map these
+# transient sub-states to `running` so a stranded drain marker reads as the
+# run-intent it actually represents. This mirrors gateway/run.py's #42675
+# handling, which persists `running` (not the mid-shutdown `draining`) when an
+# unexpected signal tears the gateway down — extended here to the case where
+# the gateway died before it could persist anything at all.
+#
+# `starting` / `startup_failed` are deliberately NOT included: those mean the
+# gateway died mid-boot or failed to come up, so auto-restarting them would
+# reintroduce the crash-loop the down-marker guard exists to prevent.
+_TRANSIENT_RUNNING_STATES = frozenset({"draining"})
+
 # Stale runtime files we sweep before recreating service slots. These
 # all hold container-namespaced state (PIDs, process tables) that's
 # garbage post-restart — a numerically-equal PID in the new container
@@ -324,6 +347,15 @@ def _read_desired_state(profile_dir: Path) -> str | None:
     that as a compatibility fallback so existing running/stopped profiles
     preserve their behavior until the next explicit start/stop.
 
+    When falling back to ``gateway_state`` (no explicit ``desired_state``),
+    a transient running sub-state (``draining``) is normalised to ``running``
+    — see ``_TRANSIENT_RUNNING_STATES``. A gateway hard-killed mid-drain
+    leaves ``draining`` as its last persisted value; without this it would be
+    treated as a non-autostart state and the gateway would stay DOWN forever.
+    An explicit ``desired_state`` is always honoured verbatim (it is the
+    operator's durable intent), so this normalisation only affects the
+    legacy/transient fallback path.
+
     Missing or unparseable files count as "no desired state" so we don't
     bork the whole reconciliation on a corrupt file.
     """
@@ -335,7 +367,10 @@ def _read_desired_state(profile_dir: Path) -> str | None:
         desired_state = data.get("desired_state")
         if desired_state is not None:
             return desired_state
-        return data.get("gateway_state")
+        gateway_state = data.get("gateway_state")
+        if gateway_state in _TRANSIENT_RUNNING_STATES:
+            return "running"
+        return gateway_state
     except (OSError, json.JSONDecodeError):
         log.warning(
             "could not read %s; treating as no prior state", state_file,
diff --git a/tests/hermes_cli/test_container_boot.py b/tests/hermes_cli/test_container_boot.py
index 9d9981cf6de..0eec6899f7a 100644
--- a/tests/hermes_cli/test_container_boot.py
+++ b/tests/hermes_cli/test_container_boot.py
@@ -229,6 +229,72 @@ def test_starting_state_does_not_autostart(tmp_path: Path) -> None:
     assert named[0].action == "registered"
 
 
+def test_draining_runtime_state_autostarts(tmp_path: Path) -> None:
+    """A gateway hard-killed mid-drain leaves `gateway_state=draining` as its
+    last persisted value (the recreate SIGTERMs it before `_stop_impl` can
+    write a terminal `stopped`/`running`). `draining` is a transient sub-state
+    of RUNNING, not an operator stop, so with no explicit `desired_state` it
+    must normalise to running-intent and auto-start — otherwise the gateway
+    stays DOWN forever and messaging silently goes dark (the relay-opted-in
+    staging wedge, 2026-06)."""
+    scandir = tmp_path / "run-service"; scandir.mkdir()
+    _make_profile(tmp_path, "drained", state="draining")
+
+    actions = reconcile_profile_gateways(
+        hermes_home=tmp_path, scandir=scandir, dry_run=False,
+    )
+
+    assert _named_actions(actions) == [ReconcileAction(
+        profile="drained", prior_state="running", action="started",
+    )]
+    # Autostart means NO down-marker — the gateway comes back up.
+    assert not (scandir / "gateway-drained" / "down").exists()
+
+
+def test_draining_default_root_autostarts(tmp_path: Path) -> None:
+    """The hosted-agent path: the default (root) profile, not a named one.
+    A managed Fly instance runs the root profile; a stranded `draining` there
+    is exactly what wedged the relay-opted-in staging instance. Mirror the
+    named-profile case for the default slot."""
+    scandir = tmp_path / "run-service"; scandir.mkdir()
+    _seed_default_root(tmp_path, state="draining")
+
+    actions = reconcile_profile_gateways(
+        hermes_home=tmp_path, scandir=scandir, dry_run=False,
+    )
+
+    default_action = next(a for a in actions if a.profile == "default")
+    assert default_action.prior_state == "running"
+    assert default_action.action == "started"
+    assert not (scandir / "gateway-default" / "down").exists()
+
+
+def test_desired_state_stopped_overrides_draining_runtime(tmp_path: Path) -> None:
+    """An explicit operator stop must survive even when the transient runtime
+    state is `draining`. The `desired_state` is the durable intent and is
+    honoured verbatim — the draining→running normalisation only applies to the
+    legacy/transient `gateway_state` fallback, never over an explicit
+    `desired_state`."""
+    scandir = tmp_path / "run-service"; scandir.mkdir()
+    _make_profile(
+        tmp_path,
+        "stopped-while-draining",
+        state="draining",
+        desired_state="stopped",
+    )
+
+    actions = reconcile_profile_gateways(
+        hermes_home=tmp_path, scandir=scandir, dry_run=False,
+    )
+
+    assert _named_actions(actions) == [ReconcileAction(
+        profile="stopped-while-draining",
+        prior_state="stopped",
+        action="registered",
+    )]
+    assert (scandir / "gateway-stopped-while-draining" / "down").exists()
+
+
 def test_stale_runtime_files_are_removed(tmp_path: Path) -> None:
     scandir = tmp_path / "run-service"; scandir.mkdir()
     profile = _make_profile(tmp_path, "coder", state="running", with_pid=True)