diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index f94f690af2..2d01ae9a85 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -126,6 +126,51 @@ RUN_BUDGET_WRAPUP_NOTICE = (
 )
 
 
+def _midturn_request_pressure_tokens(
+    agent: Any,
+    api_messages: List[Dict[str, Any]],
+    effective_system: str,
+    approx_tokens: int,
+) -> int:
+    """Token figure the mid-turn pre-API compression guard compares.
+
+    When the upcoming request is eligible for native Responses compaction the
+    transport will checkpoint-prune the payload before sending, so the generic
+    durable-history estimate overstates the wire by orders of magnitude on a
+    compacted session and fires a 600s local compression the main request
+    never needed (#96995). Mirror the turn-prologue preflight (#96644 /
+    #96155): use the pruned estimate when native eligibility is proven, the
+    generic message+tools figure otherwise.
+
+    The native estimator adds the system prompt and tool schemas itself and
+    its converter skips system-role rows, so passing the assembled
+    ``api_messages`` (which carries the system row) alongside
+    ``effective_system`` counts the system prompt exactly once.
+    """
+    try:
+        from agent.codex_responses_adapter import (
+            estimate_native_responses_preflight_tokens,
+        )
+
+        native = estimate_native_responses_preflight_tokens(
+            agent,
+            api_messages,
+            system_prompt=effective_system or "",
+            tools=getattr(agent, "tools", None) or None,
+        )
+        if isinstance(native, int) and not isinstance(native, bool) and native >= 0:
+            return native
+    except Exception:
+        logger.debug(
+            "native Responses mid-turn estimate unavailable; "
+            "using generic transcript estimate",
+            exc_info=True,
+        )
+    return approx_tokens + (
+        _estimate_tools_tokens_rough(agent.tools) if agent.tools else 0
+    )
+
+
 def _review_input_budget_exhausted(agent: Any) -> bool:
     """True when a detached review fork has replayed its aggregate input budget.
 
@@ -2608,8 +2653,14 @@ def run_conversation(
         # separately (compression needs them: 50+ tools = 20-30K tokens).
         # total_chars is a rough (~) proxy — verbose log + hook metric only.
         approx_tokens = estimate_messages_tokens_rough(api_messages)
-        request_pressure_tokens = approx_tokens + (
-            _estimate_tools_tokens_rough(agent.tools) if agent.tools else 0
+        # Route-aware pressure: when the upcoming request is eligible for
+        # native Responses compaction the transport will checkpoint-prune
+        # the payload before sending — the generic durable-history figure
+        # overstates the wire by orders of magnitude on a compacted session
+        # and fires a 600s local compression the main request never needed
+        # (#96995, mirroring the turn-prologue preflight #96644/#96155).
+        request_pressure_tokens = _midturn_request_pressure_tokens(
+            agent, api_messages, effective_system or "", approx_tokens
         )
         # Usage-anchored override: when the last provider response's exact
         # usage is still valid for the durable transcript, replace the
diff --git a/tests/agent/test_native_preflight_estimate.py b/tests/agent/test_native_preflight_estimate.py
index b26b8ec94b..307a485407 100644
--- a/tests/agent/test_native_preflight_estimate.py
+++ b/tests/agent/test_native_preflight_estimate.py
@@ -98,3 +98,51 @@ def test_preflight_wrapper_falls_back_to_generic_when_ineligible():
     generic = estimate_request_tokens_rough(messages)
 
     assert _preflight_request_tokens(agent, messages, "") == generic
+
+
+# ── Mid-turn pre-API guard parity (#96995) ────────────────────────────────
+# The mid-turn guard in conversation_loop must measure the same pruned wire
+# payload the turn-prologue preflight does (#96644/#96155); before #96995 it
+# used the generic durable-history estimate and false-tripped 600s local
+# compression on compacted native-Codex sessions.
+
+
+def test_midturn_pressure_uses_pruned_estimate_when_eligible():
+    from agent.conversation_loop import (
+        _midturn_request_pressure_tokens,
+        estimate_messages_tokens_rough,
+    )
+
+    agent = _codex_agent()
+    messages = [{"role": "system", "content": "be brief"}] + _history_with_checkpoint()
+    native = estimate_native_responses_preflight_tokens(
+        agent, messages, system_prompt="be brief"
+    )
+    generic = estimate_messages_tokens_rough(messages)
+
+    assert native is not None
+    assert generic > native * 2
+    # The assembled api_messages carry the system row; the helper must not
+    # double-count it (converter skips system rows, system_prompt adds it once).
+    assert _midturn_request_pressure_tokens(
+        agent, messages, "be brief", generic
+    ) == native
+
+
+def test_midturn_pressure_falls_back_to_generic_plus_tools_when_ineligible():
+    from agent.conversation_loop import (
+        _estimate_tools_tokens_rough,
+        _midturn_request_pressure_tokens,
+        estimate_messages_tokens_rough,
+    )
+
+    agent = _codex_agent(
+        api_mode="chat_completions",
+        tools=[{"type": "function", "function": {"name": "t", "parameters": {}}}],
+    )
+    messages = [{"role": "system", "content": "be brief"}] + _history_with_checkpoint()
+    approx = estimate_messages_tokens_rough(messages)
+
+    assert _midturn_request_pressure_tokens(
+        agent, messages, "be brief", approx
+    ) == approx + _estimate_tools_tokens_rough(agent.tools)