diff --git a/cli.py b/cli.py
index d4053c8cb9c..a815175d9fe 100644
--- a/cli.py
+++ b/cli.py
@@ -577,6 +577,7 @@ def load_cli_config() -> Dict[str, Any]:
         "docker_mount_cwd_to_workspace": "TERMINAL_DOCKER_MOUNT_CWD_TO_WORKSPACE",
         "docker_run_as_host_user": "TERMINAL_DOCKER_RUN_AS_HOST_USER",
         "docker_persist_across_processes": "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES",
+        "docker_orphan_reaper": "TERMINAL_DOCKER_ORPHAN_REAPER",
         "sandbox_dir": "TERMINAL_SANDBOX_DIR",
         # Persistent shell (non-local backends)
         "persistent_shell": "TERMINAL_PERSISTENT_SHELL",
diff --git a/gateway/run.py b/gateway/run.py
index d1b1c744d38..876a23879e1 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -832,6 +832,7 @@ if _config_path.exists():
                 "docker_mount_cwd_to_workspace": "TERMINAL_DOCKER_MOUNT_CWD_TO_WORKSPACE",
                 "docker_run_as_host_user": "TERMINAL_DOCKER_RUN_AS_HOST_USER",
                 "docker_persist_across_processes": "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES",
+                "docker_orphan_reaper": "TERMINAL_DOCKER_ORPHAN_REAPER",
                 "sandbox_dir": "TERMINAL_SANDBOX_DIR",
                 "persistent_shell": "TERMINAL_PERSISTENT_SHELL",
             }
diff --git a/hermes_cli/config.py b/hermes_cli/config.py
index f6eb69d3b80..74c04635712 100644
--- a/hermes_cli/config.py
+++ b/hermes_cli/config.py
@@ -5552,6 +5552,7 @@ def set_config_value(key: str, value: str):
         "terminal.docker_mount_cwd_to_workspace": "TERMINAL_DOCKER_MOUNT_CWD_TO_WORKSPACE",
         "terminal.docker_run_as_host_user": "TERMINAL_DOCKER_RUN_AS_HOST_USER",
         "terminal.docker_persist_across_processes": "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES",
+        "terminal.docker_orphan_reaper": "TERMINAL_DOCKER_ORPHAN_REAPER",
         "terminal.docker_env": "TERMINAL_DOCKER_ENV",
         # terminal.cwd intentionally excluded — CLI resolves at runtime,
         # gateway bridges it in gateway/run.py. Persisting to .env causes
diff --git a/tests/conftest.py b/tests/conftest.py
index fd91b558f5f..fcb19c71fb4 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -228,6 +228,7 @@ _HERMES_BEHAVIORAL_VARS = frozenset({
     "TERMINAL_CONTAINER_MEMORY",
     "TERMINAL_CONTAINER_PERSISTENT",
     "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES",
+    "TERMINAL_DOCKER_ORPHAN_REAPER",
     "TERMINAL_DOCKER_RUN_AS_HOST_USER",
     "BROWSER_CDP_URL",
     "CAMOFOX_URL",
diff --git a/tests/tools/test_docker_environment.py b/tests/tools/test_docker_environment.py
index abdce91ba5f..8073813f71c 100644
--- a/tests/tools/test_docker_environment.py
+++ b/tests/tools/test_docker_environment.py
@@ -975,3 +975,254 @@ def test_cleanup_on_env_with_no_container_id_does_not_raise(monkeypatch):
     env._home_dir = None
     # No exception expected.
     env.cleanup()
+
+
+# ── Orphan reaper (issue #20561) ──────────────────────────────────
+
+
+def _now_iso(offset_seconds: int = 0) -> str:
+    """Return an RFC3339 timestamp ``offset_seconds`` in the past."""
+    import datetime
+    t = datetime.datetime.now(datetime.timezone.utc) - datetime.timedelta(seconds=offset_seconds)
+    # Format like Docker emits — with nanoseconds-style trailing digits.
+    return t.isoformat().replace("+00:00", ".123456789Z")
+
+
+def _reaper_run_mock(monkeypatch, ps_ids: list[str], inspect_responses: dict[str, str],
+                      rm_succeeds: bool = True):
+    """Build a subprocess.run mock for reaper tests.
+
+    * ``ps_ids`` — what ``docker ps -a --filter ... --format '{{.ID}}'`` returns
+    * ``inspect_responses[cid]`` — what ``docker inspect ... FinishedAt`` returns
+      for each cid; ``""`` means "field unset".
+    * ``rm_succeeds`` — whether ``docker rm -f`` returns 0.
+
+    Captures every call so tests can assert which containers were rm'd.
+    """
+    calls = []
+
+    def _run(cmd, **kwargs):
+        calls.append((list(cmd) if isinstance(cmd, list) else cmd, kwargs))
+        if not isinstance(cmd, list) or len(cmd) < 2:
+            return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+        sub = cmd[1]
+        if sub == "ps":
+            return subprocess.CompletedProcess(
+                cmd, 0, stdout="\n".join(ps_ids) + ("\n" if ps_ids else ""), stderr="",
+            )
+        if sub == "inspect":
+            # cmd is [docker, inspect, --format, '{{.State.FinishedAt}}', cid]
+            cid = cmd[-1]
+            return subprocess.CompletedProcess(
+                cmd, 0, stdout=inspect_responses.get(cid, "") + "\n", stderr="",
+            )
+        if sub == "rm":
+            return subprocess.CompletedProcess(
+                cmd, 0 if rm_succeeds else 1,
+                stdout="", stderr="" if rm_succeeds else "no such container",
+            )
+        return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+
+    monkeypatch.setattr(docker_env.subprocess, "run", _run)
+    return calls
+
+
+def test_reap_orphan_returns_zero_when_no_matches(monkeypatch):
+    """No labeled containers → no rm calls, returns 0. Establishes the
+    happy-path baseline for the orphan reaper (issue #20561)."""
+    calls = _reaper_run_mock(monkeypatch, ps_ids=[], inspect_responses={})
+
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+
+    assert removed == 0
+    rms = [c for c in calls if isinstance(c[0], list) and c[0][1:2] == ["rm"]]
+    assert not rms, "no rm calls expected when ps returns empty"
+
+
+def test_reap_orphan_removes_stale_exited_container(monkeypatch):
+    """An Exited container older than max_age_seconds must be removed.
+    This is the core repair path for issue #20561 — without the reaper,
+    SIGKILL'd Hermes processes leak containers permanently."""
+    old = _now_iso(offset_seconds=900)  # 15 minutes ago
+    calls = _reaper_run_mock(
+        monkeypatch, ps_ids=["old-cid"], inspect_responses={"old-cid": old},
+    )
+
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+
+    assert removed == 1
+    rms = [c for c in calls if isinstance(c[0], list) and c[0][1:2] == ["rm"]]
+    assert len(rms) == 1
+    assert "old-cid" in rms[0][0], f"expected rm of old-cid, got {rms[0][0]}"
+
+
+def test_reap_orphan_spares_recently_exited_container(monkeypatch):
+    """A container exited within max_age_seconds must NOT be reaped — that
+    container belongs to a Hermes process that just finished and may be
+    about to be replaced. Conservative window prevents racing sibling
+    processes."""
+    recent = _now_iso(offset_seconds=60)  # 1 minute ago
+    calls = _reaper_run_mock(
+        monkeypatch, ps_ids=["recent-cid"], inspect_responses={"recent-cid": recent},
+    )
+
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+
+    assert removed == 0
+    rms = [c for c in calls if isinstance(c[0], list) and c[0][1:2] == ["rm"]]
+    assert not rms, f"recent container must not be reaped, got rm calls: {rms}"
+
+
+def test_reap_orphan_scopes_to_profile_filter_via_label(monkeypatch):
+    """The reaper must pass ``--filter label=hermes-profile=<profile>`` to
+    docker ps so it never sweeps another profile's containers. A research
+    profile must not tear down the default profile's stragglers."""
+    calls = _reaper_run_mock(monkeypatch, ps_ids=[], inspect_responses={})
+
+    docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="research-bot", docker_exe="/usr/bin/docker",
+    )
+
+    ps_calls = [c for c in calls if isinstance(c[0], list) and c[0][1:2] == ["ps"]]
+    assert ps_calls, "expected at least one docker ps call"
+    flat = " ".join(ps_calls[0][0])
+    assert "label=hermes-profile=research-bot" in flat, (
+        f"profile filter not applied to docker ps; got args: {ps_calls[0][0]}"
+    )
+    assert "label=hermes-agent=1" in flat, (
+        f"hermes-agent label filter must also be applied; got: {ps_calls[0][0]}"
+    )
+    assert "status=exited" in flat, (
+        "must filter to exited containers only — running containers may "
+        "belong to a sibling Hermes process and must NEVER be reaped"
+    )
+
+
+def test_reap_orphan_skips_container_with_unparseable_finished_at(monkeypatch):
+    """If docker inspect returns the zero-value ``0001-01-01T00:00:00Z`` (no
+    FinishedAt yet) or an unparseable timestamp, the reaper must leave the
+    container alone. Defensive — never reap a container whose age we can't
+    determine."""
+    calls = _reaper_run_mock(
+        monkeypatch,
+        ps_ids=["never-finished", "garbage-ts"],
+        inspect_responses={
+            "never-finished": "0001-01-01T00:00:00Z",
+            "garbage-ts": "not-a-timestamp",
+        },
+    )
+
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+
+    assert removed == 0
+    rms = [c for c in calls if isinstance(c[0], list) and c[0][1:2] == ["rm"]]
+    assert not rms, (
+        f"reaper must NOT remove containers with unparseable FinishedAt; got: {rms}"
+    )
+
+
+def test_reap_orphan_handles_docker_ps_failure_gracefully(monkeypatch):
+    """If docker ps itself fails (daemon down, permission denied), the
+    reaper returns 0 without crashing. The reaper is best-effort plumbing,
+    not a critical path — it must never block container creation."""
+    def _failing_ps(cmd, **kwargs):
+        if isinstance(cmd, list) and len(cmd) >= 2 and cmd[1] == "ps":
+            return subprocess.CompletedProcess(cmd, 1, stdout="", stderr="Cannot connect to daemon")
+        return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+
+    monkeypatch.setattr(docker_env.subprocess, "run", _failing_ps)
+
+    # Must not raise
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+    assert removed == 0
+
+
+def test_reap_orphan_continues_after_individual_rm_failure(monkeypatch):
+    """If ``docker rm -f`` fails on one container (already removed by a
+    concurrent process, container locked, etc.), the reaper must log and
+    continue to the next candidate rather than aborting the whole sweep."""
+    old = _now_iso(offset_seconds=900)
+    rm_calls = []
+
+    def _run(cmd, **kwargs):
+        if not isinstance(cmd, list) or len(cmd) < 2:
+            return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+        sub = cmd[1]
+        if sub == "ps":
+            return subprocess.CompletedProcess(
+                cmd, 0, stdout="cid-a\ncid-b\ncid-c\n", stderr="",
+            )
+        if sub == "inspect":
+            return subprocess.CompletedProcess(cmd, 0, stdout=old + "\n", stderr="")
+        if sub == "rm":
+            rm_calls.append(cmd[-1])
+            # cid-b fails; cid-a and cid-c succeed.
+            if cmd[-1] == "cid-b":
+                return subprocess.CompletedProcess(cmd, 1, stdout="", stderr="no such container")
+            return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+        return subprocess.CompletedProcess(cmd, 0, stdout="", stderr="")
+
+    monkeypatch.setattr(docker_env.subprocess, "run", _run)
+
+    removed = docker_env.reap_orphan_containers(
+        max_age_seconds=600, profile_filter="default", docker_exe="/usr/bin/docker",
+    )
+
+    # All three were attempted, two succeeded.
+    assert removed == 2
+    assert set(rm_calls) == {"cid-a", "cid-b", "cid-c"}, (
+        f"reaper must attempt all candidates even when one fails; got: {rm_calls}"
+    )
+
+
+def test_container_finished_at_parses_nanosecond_timestamp(monkeypatch):
+    """Docker emits FinishedAt with nanosecond precision (RFC3339 with up to
+    9 fractional digits), but Python's fromisoformat caps at microseconds.
+    The helper must trim the extra digits without raising — otherwise every
+    candidate gets skipped and the reaper does nothing."""
+
+    def _run(cmd, **kwargs):
+        return subprocess.CompletedProcess(
+            cmd, 0,
+            stdout="2026-05-28T13:45:00.123456789Z\n",
+            stderr="",
+        )
+
+    monkeypatch.setattr(docker_env.subprocess, "run", _run)
+
+    result = docker_env._container_finished_at("/usr/bin/docker", "test-cid")
+    assert result is not None, "must parse RFC3339 with nanoseconds"
+    import datetime
+    assert result.tzinfo == datetime.timezone.utc
+    assert result.year == 2026 and result.month == 5 and result.day == 28
+
+
+def test_container_finished_at_returns_none_on_zero_value():
+    """Docker's zero-value ``0001-01-01T00:00:00Z`` (never finished) must
+    map to None so the reaper treats the container as unreapable."""
+    # Direct test of the parsing helper — no subprocess needed since the
+    # check happens after the inspect call returns.
+    import subprocess as _subprocess
+
+    class _MockRun:
+        def __init__(self, stdout):
+            self.returncode = 0
+            self.stdout = stdout
+            self.stderr = ""
+
+    import unittest.mock
+    with unittest.mock.patch.object(
+        docker_env.subprocess, "run", return_value=_MockRun("0001-01-01T00:00:00Z\n"),
+    ):
+        result = docker_env._container_finished_at("/usr/bin/docker", "never-finished")
+    assert result is None
diff --git a/tests/tools/test_docker_orphan_reaper_integration.py b/tests/tools/test_docker_orphan_reaper_integration.py
new file mode 100644
index 00000000000..d52dbcdaec7
--- /dev/null
+++ b/tests/tools/test_docker_orphan_reaper_integration.py
@@ -0,0 +1,139 @@
+"""Integration tests for the docker orphan-reaper wiring in terminal_tool.
+
+The reaper itself is unit-tested in tests/tools/test_docker_environment.py
+under the "Orphan reaper" section. These tests cover the terminal_tool-side
+gates: once-per-process behavior, the disable flag, and the
+``lifetime_seconds`` doubling that determines the reaper's age threshold.
+
+Issue #20561 — without these gates, parallel subagents would each fire the
+reaper on container creation, and the ``terminal.docker_orphan_reaper: false``
+opt-out would silently do nothing.
+"""
+
+import os
+from unittest.mock import patch
+
+import tools.terminal_tool as terminal_tool
+
+
+def _reset_reaper_gate():
+    """Clear the once-per-process flag between tests."""
+    terminal_tool._docker_orphan_reaper_ran = False
+
+
+def test_maybe_reap_runs_once_per_process(monkeypatch):
+    """The reaper sweep must run at most once per Python interpreter.
+    Parallel subagents that each call _create_environment(env_type='docker')
+    would otherwise fire N concurrent docker ps + inspect storms against the
+    daemon and waste 5–10s of startup."""
+    _reset_reaper_gate()
+    call_count = {"reap": 0}
+
+    def _fake_reap(**kwargs):
+        call_count["reap"] += 1
+        return 0
+
+    with patch("tools.environments.docker.reap_orphan_containers", _fake_reap):
+        config = {"docker_orphan_reaper": True}
+        terminal_tool._maybe_reap_docker_orphans(config)
+        terminal_tool._maybe_reap_docker_orphans(config)
+        terminal_tool._maybe_reap_docker_orphans(config)
+
+    assert call_count["reap"] == 1, (
+        f"reaper must run exactly once per process; got {call_count['reap']} calls"
+    )
+
+
+def test_maybe_reap_respects_disable_flag(monkeypatch):
+    """``terminal.docker_orphan_reaper: false`` (via container_config) must
+    skip the sweep entirely — no docker ps, no inspect, no rm. The escape
+    hatch for operators running multiple Hermes processes in the same
+    profile."""
+    _reset_reaper_gate()
+    call_count = {"reap": 0}
+
+    def _fake_reap(**kwargs):
+        call_count["reap"] += 1
+        return 0
+
+    with patch("tools.environments.docker.reap_orphan_containers", _fake_reap):
+        terminal_tool._maybe_reap_docker_orphans({"docker_orphan_reaper": False})
+
+    assert call_count["reap"] == 0, "disabled reaper must not run any docker calls"
+    # The once-per-process gate must NOT be tripped when the reaper is
+    # disabled — that would prevent a subsequent toggle to true from working.
+    assert terminal_tool._docker_orphan_reaper_ran is False
+
+
+def test_maybe_reap_doubles_lifetime_for_max_age(monkeypatch):
+    """The reaper's age threshold is ``2 × lifetime_seconds`` (with a 60s
+    floor). Generous default — gives sibling Hermes processes ample grace
+    to be replaced without their just-exited containers being yanked."""
+    _reset_reaper_gate()
+    captured_args = {}
+
+    def _fake_reap(**kwargs):
+        captured_args.update(kwargs)
+        return 0
+
+    monkeypatch.setenv("TERMINAL_LIFETIME_SECONDS", "300")
+    with patch("tools.environments.docker.reap_orphan_containers", _fake_reap):
+        terminal_tool._maybe_reap_docker_orphans({"docker_orphan_reaper": True})
+
+    assert captured_args.get("max_age_seconds") == 600, (
+        f"expected 2 × 300 = 600, got {captured_args.get('max_age_seconds')}"
+    )
+
+
+def test_maybe_reap_floors_at_60_seconds(monkeypatch):
+    """A user pinning TERMINAL_LIFETIME_SECONDS=0 (or any value <30) would
+    otherwise get an effective age threshold of zero, which would race the
+    user's own just-started container creation. Floor at 60s × 2 = 120s."""
+    _reset_reaper_gate()
+    captured_args = {}
+
+    def _fake_reap(**kwargs):
+        captured_args.update(kwargs)
+        return 0
+
+    monkeypatch.setenv("TERMINAL_LIFETIME_SECONDS", "0")
+    with patch("tools.environments.docker.reap_orphan_containers", _fake_reap):
+        terminal_tool._maybe_reap_docker_orphans({"docker_orphan_reaper": True})
+
+    assert captured_args.get("max_age_seconds") == 120, (
+        f"expected floored 60 × 2 = 120, got {captured_args.get('max_age_seconds')}"
+    )
+
+
+def test_maybe_reap_passes_current_profile_as_filter(monkeypatch):
+    """The reaper must be scoped to the current Hermes profile — a research
+    profile must NEVER reap default's containers. Verifies the
+    profile-filter wiring."""
+    _reset_reaper_gate()
+    captured_args = {}
+
+    def _fake_reap(**kwargs):
+        captured_args.update(kwargs)
+        return 0
+
+    with patch("tools.environments.docker.reap_orphan_containers", _fake_reap), \
+         patch("tools.environments.docker._get_active_profile_name", return_value="research-bot"):
+        terminal_tool._maybe_reap_docker_orphans({"docker_orphan_reaper": True})
+
+    assert captured_args.get("profile_filter") == "research-bot", (
+        f"expected profile_filter='research-bot', got {captured_args.get('profile_filter')!r}"
+    )
+
+
+def test_maybe_reap_swallows_exceptions(monkeypatch):
+    """A reaper crash (docker daemon down, parse error in helper) must NOT
+    block env creation. The reaper is best-effort plumbing, not a critical
+    path; failures get logged at debug level and execution continues."""
+    _reset_reaper_gate()
+
+    def _exploding_reap(**kwargs):
+        raise RuntimeError("docker daemon ate the cat")
+
+    with patch("tools.environments.docker.reap_orphan_containers", _exploding_reap):
+        # Must not raise
+        terminal_tool._maybe_reap_docker_orphans({"docker_orphan_reaper": True})
diff --git a/tests/tools/test_terminal_config_env_sync.py b/tests/tools/test_terminal_config_env_sync.py
index ba15cc2670e..16131843417 100644
--- a/tests/tools/test_terminal_config_env_sync.py
+++ b/tests/tools/test_terminal_config_env_sync.py
@@ -244,3 +244,19 @@ def test_docker_persist_across_processes_is_bridged_everywhere():
     assert "docker_persist_across_processes" in _gateway_env_map_keys()
     assert "docker_persist_across_processes" in _save_config_env_sync_keys()
     assert "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES" in _terminal_tool_env_var_names()
+
+
+def test_docker_orphan_reaper_is_bridged_everywhere():
+    """Regression pin for the startup orphan reaper toggle (issue #20561).
+
+    ``terminal.docker_orphan_reaper`` controls whether Hermes sweeps stale
+    Exited containers from prior SIGKILL'd processes at startup.  Same
+    four-site bridge invariant — drift means
+    ``terminal.docker_orphan_reaper: false`` silently does nothing for one
+    entry point, and the reaper either runs when the operator disabled it
+    or fails to run when they enabled it.
+    """
+    assert "docker_orphan_reaper" in _cli_env_map_keys()
+    assert "docker_orphan_reaper" in _gateway_env_map_keys()
+    assert "docker_orphan_reaper" in _save_config_env_sync_keys()
+    assert "TERMINAL_DOCKER_ORPHAN_REAPER" in _terminal_tool_env_var_names()
diff --git a/tools/environments/docker.py b/tools/environments/docker.py
index 30eb2230957..7ab97916f30 100644
--- a/tools/environments/docker.py
+++ b/tools/environments/docker.py
@@ -133,6 +133,132 @@ def _get_active_profile_name() -> str:
         return "default"
 
 
+def reap_orphan_containers(
+    *,
+    max_age_seconds: int = 600,
+    profile_filter: str | None = None,
+    docker_exe: str | None = None,
+) -> int:
+    """Remove stale hermes-tagged containers left behind by prior processes.
+
+    Targets containers that match all of:
+
+    * ``label=hermes-agent=1`` (created by this codebase)
+    * ``status=exited`` (running containers are NEVER reaped — they may
+      belong to a sibling Hermes process whose reuse path will pick them
+      up; killing them would crash the sibling mid-command)
+    * (optional) ``label=hermes-profile=<profile_filter>`` (sweep only the
+      caller's profile by default; a hermes process in profile A must not
+      tear down profile B's containers)
+    * ``State.FinishedAt`` older than *max_age_seconds* ago (so a sibling
+      process that just exited and is about to be replaced doesn't get
+      its container yanked out from under it)
+
+    Returns the number of containers removed. Best-effort: any failure
+    (docker daemon unreachable, slow inspect, parse error) is logged at
+    debug level and the function returns whatever it managed before the
+    failure. Safe to call repeatedly; idempotent.
+
+    Issue #20561 — this is the safety net for SIGKILL / OOM / crashed
+    terminal exits that bypass the ``atexit`` cleanup hook. Without it,
+    even with the cleanup-fix in the prior commit, a hard-killed Hermes
+    process leaves its container behind permanently because there's no
+    subsequent Hermes process scheduled to reuse that exact (task, profile)
+    pair.
+    """
+    docker = docker_exe or find_docker() or "docker"
+    filters = ["--filter", "label=hermes-agent=1", "--filter", "status=exited"]
+    if profile_filter:
+        filters.extend(["--filter", f"label=hermes-profile={_sanitize_label_value(profile_filter)}"])
+
+    try:
+        listing = subprocess.run(
+            [docker, "ps", "-a", *filters, "--format", "{{.ID}}"],
+            capture_output=True, text=True, timeout=15, check=False,
+        )
+    except (subprocess.TimeoutExpired, OSError) as e:
+        logger.debug("orphan reaper docker ps failed: %s", e)
+        return 0
+    if listing.returncode != 0:
+        logger.debug(
+            "orphan reaper docker ps returned %d: %s",
+            listing.returncode, listing.stderr.strip(),
+        )
+        return 0
+
+    candidate_ids = [ln.strip() for ln in listing.stdout.splitlines() if ln.strip()]
+    if not candidate_ids:
+        return 0
+
+    # Inspect each candidate to get FinishedAt; reap only those exited
+    # long enough ago.  Doing this per-container (rather than bulk inspect)
+    # keeps the failure blast radius to one container at a time.
+    import datetime
+    now = datetime.datetime.now(datetime.timezone.utc)
+    removed = 0
+    for cid in candidate_ids:
+        finished_at = _container_finished_at(docker, cid)
+        if finished_at is None:
+            # Couldn't determine age — be conservative and leave it alone.
+            continue
+        age = (now - finished_at).total_seconds()
+        if age < max_age_seconds:
+            continue
+        try:
+            result = subprocess.run(
+                [docker, "rm", "-f", cid],
+                capture_output=True, text=True, timeout=30,
+            )
+            if result.returncode == 0:
+                removed += 1
+                logger.info(
+                    "Reaped orphan container %s (exited %d seconds ago)",
+                    cid[:12], int(age),
+                )
+            else:
+                logger.debug(
+                    "docker rm -f %s failed: %s",
+                    cid[:12], result.stderr.strip(),
+                )
+        except (subprocess.TimeoutExpired, OSError) as e:
+            logger.debug("orphan reaper docker rm %s failed: %s", cid[:12], e)
+    return removed
+
+
+def _container_finished_at(docker_exe: str, container_id: str):
+    """Parse ``docker inspect`` FinishedAt for *container_id*.
+
+    Returns a timezone-aware datetime, or ``None`` if the field is missing,
+    unparseable, or the zero-value ``0001-01-01T00:00:00Z`` Docker emits
+    for never-finished containers. ``None`` means "don't reap" — the caller
+    leaves the container alone.
+    """
+    try:
+        result = subprocess.run(
+            [docker_exe, "inspect", "--format", "{{.State.FinishedAt}}", container_id],
+            capture_output=True, text=True, timeout=10, check=False,
+        )
+    except (subprocess.TimeoutExpired, OSError) as e:
+        logger.debug("orphan reaper docker inspect %s failed: %s", container_id[:12], e)
+        return None
+    if result.returncode != 0:
+        return None
+    raw = result.stdout.strip()
+    if not raw or raw.startswith("0001-01-01"):
+        return None
+    # Docker emits RFC3339 with nanoseconds (e.g. "2026-05-28T13:45:00.123456789Z").
+    # Python's fromisoformat handles microseconds but not nanoseconds; trim.
+    import re as _re
+    raw = _re.sub(r"(\.\d{6})\d+", r"\1", raw)
+    raw = raw.replace("Z", "+00:00")
+    try:
+        import datetime
+        return datetime.datetime.fromisoformat(raw)
+    except ValueError as e:
+        logger.debug("could not parse FinishedAt %r for %s: %s", raw, container_id[:12], e)
+        return None
+
+
 def find_docker() -> Optional[str]:
     """Locate the docker (or podman) CLI binary.
 
@@ -564,7 +690,7 @@ class DockerEnvironment(BaseEnvironment):
             "hermes-profile": profile_name,
         }
 
-        # Cross-process reuse (issue #20561 — docs claim "ONE long-lived
+        # Cross-process container reuse (issue #20561 — docs claim "ONE long-lived
         # container shared across sessions").  If a prior Hermes process
         # already started a container for this (task_id, profile) and it
         # still exists, attach to it instead of starting a fresh one.  This
diff --git a/tools/terminal_tool.py b/tools/terminal_tool.py
index 513fa31b9f9..6b0d42aa886 100644
--- a/tools/terminal_tool.py
+++ b/tools/terminal_tool.py
@@ -861,6 +861,78 @@ _creation_locks_lock = threading.Lock()  # Protects _creation_locks dict itself
 _cleanup_thread = None
 _cleanup_running = False
 
+# Once-per-process guard for the docker orphan reaper (issue #20561).
+# Set when _maybe_reap_docker_orphans first runs; concurrent _create_environment
+# calls for parallel subagents won't re-trigger the sweep.
+_docker_orphan_reaper_ran = False
+_docker_orphan_reaper_lock = threading.Lock()
+
+
+def _maybe_reap_docker_orphans(container_config: Dict[str, Any]) -> None:
+    """Run the docker orphan reaper once per process, if enabled.
+
+    Sweeps long-Exited containers labeled ``hermes-agent=1`` for the current
+    profile that match the issue #20561 leak class — containers left behind
+    by Hermes processes that exited without firing ``atexit`` (SIGKILL,
+    OOM, terminal-window-close). The reaper is conservative by default:
+    only Exited containers older than ``2 × lifetime_seconds`` and scoped to
+    the current profile.
+
+    Gates:
+
+    * ``terminal.docker_orphan_reaper: false`` disables it entirely (the
+      operator opted out — usually because they're running multiple
+      Hermes processes in the same profile and don't trust the
+      conservative defaults).
+    * ``_docker_orphan_reaper_ran`` flag — sweep runs once per Python
+      interpreter, not on every subagent / RL-rollout / parallel
+      ``terminal()`` call.
+    """
+    global _docker_orphan_reaper_ran
+    if not container_config.get("docker_orphan_reaper", True):
+        return
+    # Cheap double-checked-locking: read without the lock, take the lock
+    # only on first run, recheck inside.
+    if _docker_orphan_reaper_ran:
+        return
+    with _docker_orphan_reaper_lock:
+        if _docker_orphan_reaper_ran:
+            return
+        _docker_orphan_reaper_ran = True
+
+    # 2 × lifetime_seconds gives sibling Hermes processes a generous grace
+    # window. Floor at 60s so an operator with TERMINAL_LIFETIME_SECONDS=0
+    # doesn't get an instant-reap that races their own setup.
+    # ``container_config`` only carries container_* keys, so read
+    # lifetime_seconds from the env var the rest of the module uses.
+    try:
+        lifetime = int(os.getenv("TERMINAL_LIFETIME_SECONDS", "300"))
+    except (TypeError, ValueError):
+        lifetime = 300
+    lifetime = max(60, lifetime)
+    max_age = lifetime * 2
+
+    try:
+        from tools.environments.docker import (
+            reap_orphan_containers, _get_active_profile_name,
+        )
+    except ImportError:
+        return
+    try:
+        profile = _get_active_profile_name()
+        removed = reap_orphan_containers(
+            max_age_seconds=max_age, profile_filter=profile,
+        )
+        if removed:
+            logger.info(
+                "Docker orphan reaper removed %d stale container(s) for profile %s",
+                removed, profile,
+            )
+    except Exception as e:
+        # Never fail the env-creation path because of a janitor problem.
+        logger.debug("Docker orphan reaper raised: %s", e)
+
+
 # Per-task environment overrides registry.
 # Allows environments (e.g., TerminalBench2Env) to specify a custom Docker/Modal
 # image for a specific task_id BEFORE the agent loop starts. When the terminal or
@@ -1033,6 +1105,13 @@ def _get_env_config() -> Dict[str, Any]:
         "docker_persist_across_processes": os.getenv(
             "TERMINAL_DOCKER_PERSIST_ACROSS_PROCESSES", "true"
         ).lower() in {"true", "1", "yes"},
+        # Startup orphan reaper for hermes-tagged containers left behind by
+        # crashed / SIGKILL'd previous processes that bypassed atexit.
+        # Conservative: only sweeps Exited containers older than 2× the
+        # idle-reap window AND scoped to the current profile. Issue #20561.
+        "docker_orphan_reaper": os.getenv(
+            "TERMINAL_DOCKER_ORPHAN_REAPER", "true"
+        ).lower() in {"true", "1", "yes"},
     }
 
 
@@ -1081,6 +1160,13 @@ def _create_environment(env_type: str, image: str, cwd: str, timeout: int,
         return _LocalEnvironment(cwd=cwd, timeout=timeout)
     
     elif env_type == "docker":
+        # One-shot orphan reaper: clean up labeled containers left behind by
+        # prior Hermes processes that hit SIGKILL / OOM / a closed terminal
+        # before the atexit cleanup hook could run.  Gated to once per
+        # process so concurrent _create_environment calls (parallel
+        # subagents, RL benchmarks) don't run the reaper N times.
+        # Disable via ``terminal.docker_orphan_reaper: false`` (issue #20561).
+        _maybe_reap_docker_orphans(cc)
         return _DockerEnvironment(
             image=image, cwd=cwd, timeout=timeout,
             cpu=cpu, memory=memory, disk=disk,
@@ -1773,6 +1859,7 @@ def terminal_tool(
                                 "docker_run_as_host_user": config.get("docker_run_as_host_user", False),
                                 "docker_extra_args": config.get("docker_extra_args", []),
                                 "docker_persist_across_processes": config.get("docker_persist_across_processes", True),
+                                "docker_orphan_reaper": config.get("docker_orphan_reaper", True),
                             }
 
                         local_config = None