diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index 46cbc717a7e85..9aa623bb633ec 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -21,6 +21,7 @@
 import os
 import random
 import re
+import socket
 import ssl
 import sys
 import time
@@ -1258,16 +1259,17 @@ def host_info_value(label: str) -> str:
         each message and destroying the prefix cache for the whole session,
         which is far worse than the staleness this function guards against.
 
-        Anchor on the ``User home directory:`` line that immediately precedes
-        the working-directory line in that block, and take the FIRST such
-        occurrence, so only Hermes' own emitted block can satisfy the read.
+        Anchor on the ``User home directory:`` line in the middle of that
+        block, and take the FIRST such occurrence, so only Hermes' own emitted
+        block can satisfy the read. Runtime host fields precede the anchor;
+        the working-directory field follows it.
         """
         prefix = f"{label}:"
         lines = prompt.splitlines()
         for idx, line in enumerate(lines):
             if not line.startswith("User home directory:"):
                 continue
-            for candidate in lines[idx + 1: idx + 4]:
+            for candidate in lines[max(0, idx - 3): idx + 4]:
                 if candidate.startswith(prefix):
                     return candidate[len(prefix):].strip()
         return ""
@@ -1292,6 +1294,33 @@ def host_info_value(label: str) -> str:
         if stored_cwd != str(resolve_agent_cwd()):
             return False
 
+    # Session databases can be synchronized between machines. A stored local
+    # prompt must never carry the other machine's runtime identity into this
+    # process merely because its profile name and cwd happen to match. Legacy
+    # local prompts have no hostname at all, so reject them once to upgrade the
+    # persisted snapshot. Remote/sandbox prompts intentionally omit the whole
+    # host-info block and remain reusable.
+    #
+    # Hostname is a useful human-readable signal but not a globally unique
+    # gateway identity: two cloned VMs or machines can share a hostname, and
+    # two gateway instances can run on the same host. This is host anchoring,
+    # not an authentication boundary; track a follow-up for a stable opaque
+    # per-install/runtime identity if stronger guarantees are needed.
+    stored_host = host_info_value("Host")
+    stored_hostname = host_info_value("Machine hostname")
+    if stored_host:
+        if not stored_hostname:
+            # Legacy local prompt without hostname: reject once to upgrade.
+            return False
+        try:
+            current_hostname = socket.gethostname().strip()
+        except OSError:
+            current_hostname = ""
+        # Fail closed: a local stored prompt must not silently be treated as
+        # verified when the live hostname cannot be read.
+        if not current_hostname or stored_hostname.casefold() != current_hostname.casefold():
+            return False
+
     # Detect runtime-surface drift: the stored prompt records which platform it
     # was built for (e.g. "desktop" vs "cli"). Reusing a desktop-built prompt on
     # a terminal session (or vice versa) would inject the wrong runtime hints.
diff --git a/agent/prompt_builder.py b/agent/prompt_builder.py
index f1c5ab0890a35..357f4b3cb5d3f 100644
--- a/agent/prompt_builder.py
+++ b/agent/prompt_builder.py
@@ -8,6 +8,7 @@
 import logging
 import os
 import queue
+import socket
 import sys
 import threading
 import contextvars
@@ -1406,8 +1407,8 @@ def build_environment_hints() -> str:
     """Return environment-specific guidance for the system prompt.
 
     Always emits a factual block describing the execution environment:
-    - For **local** terminal backends: the host OS, user home, current
-      working directory (plus a Windows-only note about hostname != user
+    - For **local** terminal backends: the host OS, live machine hostname,
+      user home, current working directory (plus a Windows-only note about hostname != user
       and a Windows-only note that `terminal` shells out to bash, not
       PowerShell).
     - For **remote / sandbox** terminal backends (docker, singularity,
@@ -1439,6 +1440,12 @@ def build_environment_hints() -> str:
         else:
             host_lines.append(f"Host: {platform.system()} ({platform.release()})")
 
+        try:
+            hostname = socket.gethostname().strip()
+        except OSError:
+            hostname = ""
+        if hostname:
+            host_lines.append(f"Machine hostname: {hostname}")
         host_lines.append(f"User home directory: {os.path.expanduser('~')}")
         try:
             host_lines.append(f"Current working directory: {resolve_agent_cwd()}")
diff --git a/tests/agent/test_prompt_builder.py b/tests/agent/test_prompt_builder.py
index 4331c2bc9d287..5cf73f487ee88 100644
--- a/tests/agent/test_prompt_builder.py
+++ b/tests/agent/test_prompt_builder.py
@@ -763,6 +763,45 @@ def test_build_environment_hints_suppresses_host_on_docker_backend(self, monkeyp
         assert "Terminal backend: docker" in result
         assert "inside" in result.lower()
 
+    def test_build_environment_hints_identifies_live_machine(self, monkeypatch):
+        """The prompt must identify the process host, not synchronized state."""
+        import agent.prompt_builder as _pb
+
+        monkeypatch.setenv("TERMINAL_ENV", "local")
+        monkeypatch.setattr("socket.gethostname", lambda: "atlas")
+
+        result = _pb.build_environment_hints()
+
+        assert "Machine hostname: atlas" in result
+        assert result.index("Machine hostname: atlas") < result.index("User home directory:")
+
+    def test_build_environment_hints_omits_hostname_when_gethostname_raises(self, monkeypatch):
+        """Regression: if socket.gethostname() raises OSError, the prompt must still build."""
+        import agent.prompt_builder as _pb
+
+        def _raise_oserror():
+            raise OSError("gethostname failed")
+
+        monkeypatch.setenv("TERMINAL_ENV", "local")
+        monkeypatch.setattr("socket.gethostname", _raise_oserror)
+
+        result = _pb.build_environment_hints()
+
+        assert "Machine hostname:" not in result
+        assert "User home directory:" in result
+
+    def test_build_environment_hints_omits_hostname_when_gethostname_returns_empty(self, monkeypatch):
+        """Regression: if socket.gethostname() returns empty string, omit the hostname line."""
+        import agent.prompt_builder as _pb
+
+        monkeypatch.setenv("TERMINAL_ENV", "local")
+        monkeypatch.setattr("socket.gethostname", lambda: "")
+
+        result = _pb.build_environment_hints()
+
+        assert "Machine hostname:" not in result
+        assert "User home directory:" in result
+
     def test_build_environment_hints_uses_terminal_cwd_over_launch_dir(self, monkeypatch, tmp_path):
         """THE BUG: gateway/cron set TERMINAL_CWD but the prompt emitted os.getcwd()
         (the daemon launch dir). Regression for #24882/#24969/#27383/#29265."""
diff --git a/tests/run_agent/test_compression_persistence.py b/tests/run_agent/test_compression_persistence.py
index a99448d1cbb28..7d127dc40c294 100644
--- a/tests/run_agent/test_compression_persistence.py
+++ b/tests/run_agent/test_compression_persistence.py
@@ -17,6 +17,7 @@
 """
 
 import os
+import socket
 import tempfile
 from pathlib import Path
 from unittest.mock import patch
@@ -390,7 +391,7 @@ class _Agent:
         return agent
 
     @staticmethod
-    def _host_block(cwd: str) -> str:
+    def _host_block(cwd: str, hostname: str | None = None) -> str:
         """A stored prompt fragment shaped like the real host-info block.
 
         ``build_environment_hints`` always emits ``User home directory:``
@@ -401,10 +402,108 @@ def _host_block(cwd: str) -> str:
         """
         return (
             "Host: Linux (6.16.0)\n"
+            f"Machine hostname: {hostname or socket.gethostname()}\n"
             "User home directory: /home/tester\n"
             f"Current working directory: {cwd}\n"
         )
 
+    def test_stored_prompt_stale_when_machine_hostname_differs(self):
+        """A session DB copied from another host must rebuild its prompt."""
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        stored_prompt = self._host_block("/project/current", hostname="personal-pc")
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", return_value="atlas"),
+        ):
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is False
+
+    def test_stored_prompt_fresh_when_machine_hostname_matches(self):
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        stored_prompt = (
+            self._host_block("/project/current", hostname="atlas")
+            + "\n# AGENTS.md\nMachine hostname: personal-pc\n"
+        )
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", return_value="atlas"),
+        ):
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is True
+
+    def test_legacy_local_prompt_without_machine_hostname_is_rebuilt(self):
+        """One rebuild upgrades pre-runtime-identity prompt snapshots."""
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        stored_prompt = (
+            "Host: Linux (6.16.0)\n"
+            "User home directory: /home/tester\n"
+            "Current working directory: /project/current\n"
+        )
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", return_value="atlas"),
+        ):
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is False
+
+    def test_stored_prompt_rejected_when_gethostname_raises_oserror(self):
+        """Fail closed: if socket.gethostname() raises OSError, reject the stored prompt."""
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        stored_prompt = self._host_block("/project/current", hostname="atlas")
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", side_effect=OSError("gethostname failed")),
+        ):
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is False
+
+    def test_stored_prompt_rejected_when_gethostname_returns_empty(self):
+        """Fail closed: if socket.gethostname() returns empty string, reject the stored prompt."""
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        stored_prompt = self._host_block("/project/current", hostname="atlas")
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", return_value=""),
+        ):
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is False
+
+    def test_same_hostname_different_profile_still_valid(self):
+        """Hostname is host anchoring, not authentication: same host, different profile is valid."""
+        from unittest.mock import patch
+        from agent.conversation_loop import _stored_prompt_matches_runtime
+
+        agent = self._make_agent()
+        # Same hostname but different user home (different profile)
+        stored_prompt = (
+            "Host: Linux (6.16.0)\n"
+            "Machine hostname: atlas\n"
+            "User home directory: /home/other-profile\n"
+            "Current working directory: /project/current\n"
+        )
+
+        with (
+            patch("agent.conversation_loop.resolve_agent_cwd", return_value="/project/current"),
+            patch("socket.gethostname", return_value="atlas"),
+        ):
+            # Same hostname should be considered valid even with different profile
+            assert _stored_prompt_matches_runtime(agent, stored_prompt) is True
+
     def test_stored_prompt_stale_when_cwd_differs(self):
         """Different cwd should force a prompt rebuild."""
         from unittest.mock import patch