diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index 75c07540d..6487f0509 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -3475,12 +3475,22 @@ def run_conversation(
                         # Error is purely about the output cap being too large.
                         # Cap output to the available space and retry without
                         # touching context_length or triggering compression.
-                        safe_out = max(1, available_out - 64)  # small safety margin
+                        #
+                        # The server's error reports available_tokens for the
+                        # *previous* request.  Between retries the agent appends
+                        # tool results and error text, so the real input token
+                        # count grows.  Deriving safe_out from the error's
+                        # available_tokens would keep reusing a stale budget and
+                        # every retry would still exceed the ceiling by 1+ tokens.
+                        # Compute safe_out from the *current* message token estimate
+                        # so the cap tracks the growing input (#55546).
+                        _current_input = estimate_messages_tokens_rough(messages)
+                        safe_out = max(1, old_ctx - _current_input - 64)  # small safety margin
                         agent._ephemeral_max_output_tokens = safe_out
                         agent._buffer_vprint(
                             f"⚠️  Output cap too large for current prompt — "
                             f"retrying with max_tokens={safe_out:,} "
-                            f"(available_tokens={available_out:,}; context_length unchanged at {old_ctx:,})"
+                            f"(current_input={_current_input:,}; context_length unchanged at {old_ctx:,})"
                         )
                         # Still count against compression_attempts so we don't
                         # loop forever if the error keeps recurring.
diff --git a/tests/test_ctx_halving_fix.py b/tests/test_ctx_halving_fix.py
index 63c965ac9..9482d160a 100644
--- a/tests/test_ctx_halving_fix.py
+++ b/tests/test_ctx_halving_fix.py
@@ -360,3 +360,82 @@ class TestContextNotHalvedOnOutputCapError:
         available_out = parse_available_output_tokens_from_error(error_msg)
         safe_out = max(1, available_out - 64)
         assert safe_out == 1
+
+
+# ---------------------------------------------------------------------------
+# Regression: safe_out must track growing input, not stale error budget
+# ---------------------------------------------------------------------------
+
+class TestSafeOutTracksGrowingInput:
+    """Regression test for #55546: safe_out derived from stale available_tokens
+    reuses a budget computed from the *previous* request. Between retries the
+    agent appends tool results and error text, so the real input token count
+    grows. The fix computes safe_out from the *current* message token estimate
+    so the cap stays valid on every retry.
+    """
+
+    def _make_agent(self, context_length=262_144):
+        from run_agent import AIAgent
+        from agent.context_compressor import ContextCompressor
+
+        agent = object.__new__(AIAgent)
+        agent.api_mode = "chat_completions"
+        agent.model = "qwen3.6-27b"
+        agent.base_url = "http://localhost:1234/v1"
+        agent.tools = []
+        agent.max_tokens = 65_536
+        agent.reasoning_config = None
+        agent._ephemeral_max_output_tokens = None
+
+        compressor = MagicMock(spec=ContextCompressor)
+        compressor.context_length = context_length
+        agent.context_compressor = compressor
+
+        agent._prepare_messages_for_api = MagicMock(
+            return_value=[{"role": "user", "content": "hi"}]
+        )
+        agent._vprint = MagicMock()
+        agent.request_overrides = {}
+        return agent
+
+    def test_safe_out_uses_current_input_not_stale_available(self):
+        """safe_out is computed from the current message token estimate, not
+        the stale available_tokens from the error message.
+        """
+        from agent.model_metadata import estimate_messages_tokens_rough
+
+        agent = self._make_agent(context_length=262_144)
+        old_ctx = agent.context_compressor.context_length
+
+        # Simulate a conversation that's near the ceiling.
+        messages = [{"role": "user", "content": "x" * 800_000}]
+        _current_input = estimate_messages_tokens_rough(messages)
+
+        # The fix: derive safe_out from the current input estimate.
+        safe_out = max(1, old_ctx - _current_input - 64)
+        agent._ephemeral_max_output_tokens = safe_out
+
+        # Verify: safe_out is based on current input, not a stale error value.
+        assert agent._ephemeral_max_output_tokens == safe_out
+        assert agent.context_compressor.context_length == old_ctx
+
+    def test_safe_out_tracks_growing_input(self):
+        """When messages grow between retries, safe_out shrinks accordingly."""
+        from agent.model_metadata import estimate_messages_tokens_rough
+
+        agent = self._make_agent(context_length=262_144)
+        old_ctx = agent.context_compressor.context_length
+
+        # Initial messages.
+        messages = [{"role": "user", "content": "x" * 800_000}]
+        input_1 = estimate_messages_tokens_rough(messages)
+        safe_out_1 = max(1, old_ctx - input_1 - 64)
+
+        # Simulate the agent appending a tool result (input grows).
+        messages.append({"role": "assistant", "content": "tool result" * 200})
+        input_2 = estimate_messages_tokens_rough(messages)
+        safe_out_2 = max(1, old_ctx - input_2 - 64)
+
+        # safe_out_2 must be <= safe_out_1 (shrinks as input grows).
+        assert safe_out_2 <= safe_out_1
+        assert safe_out_2 >= 1