diff --git a/gateway/platforms/api_server.py b/gateway/platforms/api_server.py
index 88fe3d7cd5..228a17d1e3 100644
--- a/gateway/platforms/api_server.py
+++ b/gateway/platforms/api_server.py
@@ -2081,12 +2081,13 @@ class APIServerAdapter(BasePlatformAdapter):
         """Resolve + validate the /p/<profile>/ URL prefix on an API request.
 
         Returns:
-          - ``None`` when no profile prefix is present, or multiplexing is off
-            (the prefix is ignored; request handled as the default profile).
+          - ``None`` when no profile prefix is present, or when multiplexing
+            is off and the prefix names this process's own profile (the
+            request is already scoped to the only agent served here).
           - the profile name (str) when present, multiplexing is on, and the
             profile is one this gateway serves.
-          - ``_PROFILE_REJECTED`` when a prefix is present but the profile is
-            unknown/unconfigured (handler/middleware returns 404).
+          - ``_PROFILE_REJECTED`` when a prefix is present but names a profile
+            this process cannot serve (handler/middleware returns 404).
         """
         profile = (request.match_info.get("profile") or "").strip()
         if not profile:
@@ -2094,9 +2095,25 @@ class APIServerAdapter(BasePlatformAdapter):
         runner = getattr(self, "gateway_runner", None)
         cfg = getattr(runner, "config", None)
         if not getattr(cfg, "multiplex_profiles", False):
-            # Prefix supplied but multiplexing is off — ignore it, behave as
-            # the single-profile gateway (don't 404 a would-be valid route).
-            return None
+            # A prefix names a specific agent. With multiplexing off this
+            # process serves exactly one, so honor the prefix only when it
+            # names that one (peers address single-profile daemons this way
+            # without knowing the host's topology). Anything else must fail
+            # closed: answering as the local profile would deliver the
+            # request to a DIFFERENT agent than the one addressed — silent
+            # misdelivery, strictly worse than a 404. Observed live (Aug
+            # 2026): `hermes peer dm mini/researcher` answered by the mini's
+            # default agent, with no error anywhere.
+            try:
+                from hermes_cli.profiles import get_active_profile_name
+
+                own = get_active_profile_name()
+            except Exception:
+                return _PROFILE_REJECTED
+            if profile == own:
+                # Scoped to self: same handling as no prefix at all.
+                return None
+            return _PROFILE_REJECTED
         try:
             from hermes_cli.profiles import profiles_to_serve
 
diff --git a/tests/gateway/test_api_server_profile_prefix_misdelivery.py b/tests/gateway/test_api_server_profile_prefix_misdelivery.py
new file mode 100644
index 0000000000..bc37872db9
--- /dev/null
+++ b/tests/gateway/test_api_server_profile_prefix_misdelivery.py
@@ -0,0 +1,115 @@
+"""A ``/p/<profile>/`` prefix on a non-multiplexed gateway must not misdeliver.
+
+The prefix is an address: the caller is naming WHICH agent the request is
+for. The old behavior ignored it whenever ``gateway.multiplex_profiles`` was
+off and answered as the process's own (single) profile — so a request
+explicitly addressed to one agent was silently answered by a different one.
+Observed live (Aug 2026): ``hermes peer dm mini/researcher`` was answered by
+the mini's *default* agent, with no error on either side, because the mini
+runs one LaunchDaemon per profile and only the default daemon hosted an
+api_server.
+
+The contract now: with multiplexing off, a prefix naming this process's own
+profile is honored (peers address single-profile daemons this way without
+knowing the host's topology); any other name fails closed with the existing
+404, because a wrong-agent answer is strictly worse than an error.
+"""
+
+from __future__ import annotations
+
+from types import SimpleNamespace
+
+import pytest
+from aiohttp import web
+from aiohttp.test_utils import TestClient, TestServer
+
+from gateway.platforms.api_server import _PROFILE_REJECTED, APIServerAdapter
+from gateway.config import PlatformConfig
+
+
+@pytest.fixture()
+def adapter():
+    # No gateway_runner configured -> multiplex_profiles is falsy, the exact
+    # shape of a standalone single-profile daemon.
+    return APIServerAdapter(PlatformConfig(enabled=True))
+
+
+def _request(profile: str | None):
+    return SimpleNamespace(match_info={} if profile is None else {"profile": profile})
+
+
+class TestResolverWithMultiplexOff:
+    def test_no_prefix_is_untouched(self, adapter):
+        assert adapter._resolve_request_profile(_request(None)) is None
+
+    def test_prefix_naming_own_profile_is_honored(self, adapter, monkeypatch):
+        monkeypatch.setattr(
+            "hermes_cli.profiles.get_active_profile_name", lambda: "researcher"
+        )
+        assert adapter._resolve_request_profile(_request("researcher")) is None
+
+    def test_prefix_naming_default_on_default_home_is_honored(self, adapter, monkeypatch):
+        monkeypatch.setattr(
+            "hermes_cli.profiles.get_active_profile_name", lambda: "default"
+        )
+        assert adapter._resolve_request_profile(_request("default")) is None
+
+    def test_prefix_naming_another_agent_fails_closed(self, adapter, monkeypatch):
+        """The misdelivery case: addressed to researcher, running as default."""
+        monkeypatch.setattr(
+            "hermes_cli.profiles.get_active_profile_name", lambda: "default"
+        )
+        assert adapter._resolve_request_profile(_request("researcher")) is _PROFILE_REJECTED
+
+    def test_unresolvable_own_identity_fails_closed(self, adapter, monkeypatch):
+        """If the process cannot prove who it is, it must not answer as anyone."""
+
+        def boom():
+            raise RuntimeError("no home")
+
+        monkeypatch.setattr("hermes_cli.profiles.get_active_profile_name", boom)
+        assert adapter._resolve_request_profile(_request("researcher")) is _PROFILE_REJECTED
+
+
+class TestMultiplexOnUnchanged:
+    def test_served_profile_resolves(self, adapter, monkeypatch):
+        adapter.gateway_runner = SimpleNamespace(
+            config=SimpleNamespace(
+                multiplex_profiles=True, multiplex_profile_allowlist=None
+            )
+        )
+        monkeypatch.setattr(
+            "hermes_cli.profiles.profiles_to_serve",
+            lambda multiplex, profile_allowlist: [("worker", object())],
+        )
+        assert adapter._resolve_request_profile(_request("worker")) == "worker"
+        assert adapter._resolve_request_profile(_request("ghost")) is _PROFILE_REJECTED
+
+
+@pytest.mark.asyncio
+async def test_http_request_addressed_to_another_agent_is_404_not_answered(
+    adapter, monkeypatch
+):
+    """End to end through the real middleware: the wrong-agent request must
+    404 instead of being served — a body would mean the misdelivery is back."""
+    monkeypatch.setattr(
+        "hermes_cli.profiles.get_active_profile_name", lambda: "default"
+    )
+
+    async def handler(request):
+        return web.json_response({"served_by": "default"})
+
+    app = web.Application(middlewares=[adapter._make_profile_prefix_middleware()])
+    app.router.add_get("/p/{profile}/v1/test", handler)
+    app.router.add_get("/v1/test", handler)
+
+    async with TestClient(TestServer(app)) as cli:
+        # Addressed to a different agent: refused.
+        resp = await cli.get("/p/researcher/v1/test")
+        assert resp.status == 404
+        body = await resp.json()
+        assert "profile" in str(body.get("error", "")).lower()
+
+        # Addressed to this agent, and unaddressed: both served.
+        assert (await cli.get("/p/default/v1/test")).status == 200
+        assert (await cli.get("/v1/test")).status == 200