diff --git a/gateway/run.py b/gateway/run.py
index 8458bb9d46..72ec62b409 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -1083,6 +1083,8 @@ class GatewayRunner:
                                 self.session_store.rewrite_transcript(
                                     session_entry.session_id, _compressed
                                 )
+                                # Reset stored token count — transcript was rewritten
+                                session_entry.last_prompt_tokens = 0
                                 history = _compressed
                                 _new_count = len(_compressed)
                                 _new_tokens = estimate_messages_tokens_rough(
@@ -1747,6 +1749,8 @@ class GatewayRunner:
         # Truncate history to before the last user message and persist
         truncated = history[:last_user_idx]
         self.session_store.rewrite_transcript(session_entry.session_id, truncated)
+        # Reset stored token count — transcript was truncated
+        session_entry.last_prompt_tokens = 0
         
         # Re-send by creating a fake text event with the old message
         retry_event = MessageEvent(
@@ -1778,6 +1782,8 @@ class GatewayRunner:
         removed_msg = history[last_user_idx].get("content", "")
         removed_count = len(history) - last_user_idx
         self.session_store.rewrite_transcript(session_entry.session_id, history[:last_user_idx])
+        # Reset stored token count — transcript was truncated
+        session_entry.last_prompt_tokens = 0
         
         preview = removed_msg[:40] + "..." if len(removed_msg) > 40 else removed_msg
         return f"↩️ Undid {removed_count} message(s).\nRemoved: \"{preview}\""
@@ -1911,6 +1917,10 @@ class GatewayRunner:
             )
 
             self.session_store.rewrite_transcript(session_entry.session_id, compressed)
+            # Reset stored token count — transcript changed, old value is stale
+            self.session_store.update_session(
+                session_entry.session_key, last_prompt_tokens=0,
+            )
             new_count = len(compressed)
             new_tokens = estimate_messages_tokens_rough(compressed)
 
diff --git a/gateway/session.py b/gateway/session.py
index e2777fe1a2..b1cdefa5b5 100644
--- a/gateway/session.py
+++ b/gateway/session.py
@@ -556,7 +556,7 @@ class SessionStore:
         session_key: str,
         input_tokens: int = 0,
         output_tokens: int = 0,
-        last_prompt_tokens: int = 0,
+        last_prompt_tokens: int = None,
     ) -> None:
         """Update a session's metadata after an interaction."""
         self._ensure_loaded()
@@ -566,7 +566,7 @@ class SessionStore:
             entry.updated_at = datetime.now()
             entry.input_tokens += input_tokens
             entry.output_tokens += output_tokens
-            if last_prompt_tokens > 0:
+            if last_prompt_tokens is not None:
                 entry.last_prompt_tokens = last_prompt_tokens
             entry.total_tokens = entry.input_tokens + entry.output_tokens
             self._save()
diff --git a/tests/gateway/test_session.py b/tests/gateway/test_session.py
index 562c580973..7a7f4b878c 100644
--- a/tests/gateway/test_session.py
+++ b/tests/gateway/test_session.py
@@ -429,3 +429,119 @@ class TestHasAnySessions:
 
         store._entries = {"key1": MagicMock()}
         assert store.has_any_sessions() is False
+
+
+class TestLastPromptTokens:
+    """Tests for the last_prompt_tokens field — actual API token tracking."""
+
+    def test_session_entry_default(self):
+        """New sessions should have last_prompt_tokens=0."""
+        from gateway.session import SessionEntry
+        from datetime import datetime
+        entry = SessionEntry(
+            session_key="test",
+            session_id="s1",
+            created_at=datetime.now(),
+            updated_at=datetime.now(),
+        )
+        assert entry.last_prompt_tokens == 0
+
+    def test_session_entry_roundtrip(self):
+        """last_prompt_tokens should survive serialization/deserialization."""
+        from gateway.session import SessionEntry
+        from datetime import datetime
+        entry = SessionEntry(
+            session_key="test",
+            session_id="s1",
+            created_at=datetime.now(),
+            updated_at=datetime.now(),
+            last_prompt_tokens=42000,
+        )
+        d = entry.to_dict()
+        assert d["last_prompt_tokens"] == 42000
+        restored = SessionEntry.from_dict(d)
+        assert restored.last_prompt_tokens == 42000
+
+    def test_session_entry_from_old_data(self):
+        """Old session data without last_prompt_tokens should default to 0."""
+        from gateway.session import SessionEntry
+        data = {
+            "session_key": "test",
+            "session_id": "s1",
+            "created_at": "2025-01-01T00:00:00",
+            "updated_at": "2025-01-01T00:00:00",
+            "input_tokens": 100,
+            "output_tokens": 50,
+            "total_tokens": 150,
+            # No last_prompt_tokens — old format
+        }
+        entry = SessionEntry.from_dict(data)
+        assert entry.last_prompt_tokens == 0
+
+    def test_update_session_sets_last_prompt_tokens(self, tmp_path):
+        """update_session should store the actual prompt token count."""
+        config = GatewayConfig()
+        with patch("gateway.session.SessionStore._ensure_loaded"):
+            store = SessionStore(sessions_dir=tmp_path, config=config)
+        store._loaded = True
+        store._db = None
+        store._save = MagicMock()
+
+        from gateway.session import SessionEntry
+        from datetime import datetime
+        entry = SessionEntry(
+            session_key="k1",
+            session_id="s1",
+            created_at=datetime.now(),
+            updated_at=datetime.now(),
+        )
+        store._entries = {"k1": entry}
+
+        store.update_session("k1", last_prompt_tokens=85000)
+        assert entry.last_prompt_tokens == 85000
+
+    def test_update_session_none_does_not_change(self, tmp_path):
+        """update_session with default (None) should not change last_prompt_tokens."""
+        config = GatewayConfig()
+        with patch("gateway.session.SessionStore._ensure_loaded"):
+            store = SessionStore(sessions_dir=tmp_path, config=config)
+        store._loaded = True
+        store._db = None
+        store._save = MagicMock()
+
+        from gateway.session import SessionEntry
+        from datetime import datetime
+        entry = SessionEntry(
+            session_key="k1",
+            session_id="s1",
+            created_at=datetime.now(),
+            updated_at=datetime.now(),
+            last_prompt_tokens=50000,
+        )
+        store._entries = {"k1": entry}
+
+        store.update_session("k1")  # No last_prompt_tokens arg
+        assert entry.last_prompt_tokens == 50000  # unchanged
+
+    def test_update_session_zero_resets(self, tmp_path):
+        """update_session with last_prompt_tokens=0 should reset the field."""
+        config = GatewayConfig()
+        with patch("gateway.session.SessionStore._ensure_loaded"):
+            store = SessionStore(sessions_dir=tmp_path, config=config)
+        store._loaded = True
+        store._db = None
+        store._save = MagicMock()
+
+        from gateway.session import SessionEntry
+        from datetime import datetime
+        entry = SessionEntry(
+            session_key="k1",
+            session_id="s1",
+            created_at=datetime.now(),
+            updated_at=datetime.now(),
+            last_prompt_tokens=85000,
+        )
+        store._entries = {"k1": entry}
+
+        store.update_session("k1", last_prompt_tokens=0)
+        assert entry.last_prompt_tokens == 0