diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index 3425f0970f5..7c85ae8ff54 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -4944,12 +4944,17 @@ def run_conversation(
                         getattr(agent, "_verification_stop_nudges", 0) + 1
                     )
                     final_msg["finish_reason"] = "verification_required"
+                    final_msg["_verification_stop_synthetic"] = True
                     messages.append(final_msg)
                     # Keep the attempted final answer in model history so the
                     # synthetic user nudge preserves role alternation, but do
                     # not surface it to the user as an interim answer. The
                     # whole point of this guard is to prevent premature
-                    # "done" claims before checks run.
+                    # "done" claims before checks run. Both the attempted
+                    # answer and the nudge are flagged synthetic so neither
+                    # persists — otherwise the resumed transcript keeps a
+                    # premature "done" with the nudge stripped, producing an
+                    # assistant→assistant adjacency. (#55733)
                     messages.append({
                         "role": "user",
                         "content": _verify_nudge,
@@ -4998,9 +5003,11 @@ def run_conversation(
                 if _verify_nudge2:
                     agent._pre_verify_nudges = _attempt + 1
                     final_msg["finish_reason"] = "verify_hook_continue"
+                    final_msg["_pre_verify_synthetic"] = True
                     # Same alternation contract as verify-on-stop: keep the
                     # attempted answer in history, follow it with a synthetic
-                    # user nudge, and don't surface the premature answer.
+                    # user nudge, and don't surface the premature answer. Both
+                    # are flagged synthetic so neither persists. (#55733)
                     messages.append(final_msg)
                     messages.append({
                         "role": "user",
diff --git a/run_agent.py b/run_agent.py
index 18e9f8e0c40..9b8078a5147 100644
--- a/run_agent.py
+++ b/run_agent.py
@@ -225,6 +225,13 @@ _EPHEMERAL_SCAFFOLDING_FLAGS = (
     "_empty_recovery_synthetic",
     "_empty_terminal_sentinel",
     "_thinking_prefill",
+    # verify-on-stop and pre_verify nudges append a synthetic assistant
+    # "done" plus a synthetic user nudge to keep the agent going one more
+    # turn before it can claim completion. Those messages exist only to
+    # drive the verification loop; persisting them poisons the resumed
+    # transcript and breaks prompt-prefix cache reuse on later turns. (#55733)
+    "_verification_stop_synthetic",
+    "_pre_verify_synthetic",
 )
 
 
diff --git a/tests/agent/test_verification_stop_caching.py b/tests/agent/test_verification_stop_caching.py
new file mode 100644
index 00000000000..41fee3b3374
--- /dev/null
+++ b/tests/agent/test_verification_stop_caching.py
@@ -0,0 +1,110 @@
+"""Verification-loop synthetic scaffolding must never reach durable session state.
+
+verify_on_stop / pre_verify append a synthetic assistant "done" plus a synthetic
+user nudge to keep the agent going one more turn before it can claim completion.
+These messages exist only to drive the loop; persisting them poisons the resumed
+transcript and breaks prompt-prefix cache reuse on later turns (#55733).
+
+Both persistence sinks (SQLite flush + JSON snapshot) route through the single
+``_is_ephemeral_scaffolding`` chokepoint, which is driven by
+``_EPHEMERAL_SCAFFOLDING_FLAGS``. These tests assert that the verification-loop
+flags are registered there and that both sinks drop the flagged messages while
+keeping the real conversation.
+"""
+
+import json
+import sys
+from unittest.mock import MagicMock
+
+import pytest
+
+
+def _fresh_run_agent(hermes_home):
+    for mod in list(sys.modules):
+        if mod == "run_agent" or mod.startswith("agent.") or mod.startswith("tools.") or mod.startswith("hermes_"):
+            del sys.modules[mod]
+    import run_agent  # noqa: F401
+    return sys.modules["run_agent"]
+
+
+def test_verification_flags_registered_as_ephemeral(tmp_path, monkeypatch):
+    monkeypatch.setenv("HERMES_HOME", str(tmp_path / ".hermes"))
+    ra = _fresh_run_agent(tmp_path)
+
+    assert "_verification_stop_synthetic" in ra._EPHEMERAL_SCAFFOLDING_FLAGS
+    assert "_pre_verify_synthetic" in ra._EPHEMERAL_SCAFFOLDING_FLAGS
+
+    # The central classifier drives both persistence sinks.
+    assert ra._is_ephemeral_scaffolding(
+        {"role": "assistant", "content": "done", "_verification_stop_synthetic": True}
+    )
+    assert ra._is_ephemeral_scaffolding(
+        {"role": "user", "content": "[System: run tests]", "_pre_verify_synthetic": True}
+    )
+    # Real messages are not scaffolding.
+    assert not ra._is_ephemeral_scaffolding({"role": "user", "content": "hi"})
+
+
+def _make_agent(ra, session_id, tmp_path):
+    agent = ra.AIAgent(
+        session_id=session_id,
+        api_key="test-key",
+        base_url="http://127.0.0.1:8000/v1",
+        provider="openai-compat",
+        model="test-model",
+        quiet_mode=True,
+        skip_context_files=True,
+        skip_memory=True,
+    )
+    agent._session_db = MagicMock()
+    agent._session_db_created = True
+    agent._session_json_enabled = True
+    agent.logs_dir = tmp_path / "logs"
+    agent.logs_dir.mkdir(parents=True, exist_ok=True)
+    return agent
+
+
+def test_db_flush_drops_verification_scaffolding(tmp_path, monkeypatch):
+    monkeypatch.setenv("HERMES_HOME", str(tmp_path / ".hermes"))
+    ra = _fresh_run_agent(tmp_path)
+    agent = _make_agent(ra, "sess_db", tmp_path)
+
+    messages = [
+        {"role": "user", "content": "hi"},
+        {"role": "assistant", "content": "premature done", "_verification_stop_synthetic": True},
+        {"role": "user", "content": "[System: run tests]", "_verification_stop_synthetic": True},
+        {"role": "assistant", "content": "verified and clean"},
+    ]
+
+    agent._flush_messages_to_session_db(messages, conversation_history=[])
+
+    persisted = [
+        kwargs.get("content")
+        for _args, kwargs in agent._session_db.append_message.call_args_list
+    ]
+    assert "hi" in persisted
+    assert "verified and clean" in persisted
+    assert "premature done" not in persisted
+    assert "[System: run tests]" not in persisted
+
+
+def test_json_log_drops_verification_scaffolding(tmp_path, monkeypatch):
+    monkeypatch.setenv("HERMES_HOME", str(tmp_path / ".hermes"))
+    ra = _fresh_run_agent(tmp_path)
+    agent = _make_agent(ra, "sess_json", tmp_path)
+
+    messages = [
+        {"role": "user", "content": "hi"},
+        {"role": "assistant", "content": "premature done", "_pre_verify_synthetic": True},
+        {"role": "user", "content": "[System: run tests]", "_pre_verify_synthetic": True},
+        {"role": "assistant", "content": "verified and clean"},
+    ]
+
+    agent._save_session_log(messages)
+
+    log_file = agent.logs_dir / "session_sess_json.json"
+    assert log_file.exists()
+    data = json.loads(log_file.read_text(encoding="utf-8"))
+    contents = [m.get("content") for m in data["messages"]]
+    assert contents == ["hi", "verified and clean"]
+    assert all(not m.get("_pre_verify_synthetic") for m in data["messages"])