diff --git a/agent/context_compressor.py b/agent/context_compressor.py
index 9f2b8d18b29..a51a65d11bb 100644
--- a/agent/context_compressor.py
+++ b/agent/context_compressor.py
@@ -2910,6 +2910,33 @@ This compaction should PRIORITISE preserving all information related to the focu
         # is not role=user, so we must pin the summary to "user" and
         # prevent the flip logic below from reverting it (#52160).
         _force_user_leading = last_head_role == "system"
+        # Zero-user-turn guard (#58753). The #52160 guard above only fires
+        # when the system prompt sits *inside* ``messages`` (the gateway
+        # ``/compress`` path). The main auto-compression path passes the
+        # transcript WITHOUT the system prompt (it is prepended at
+        # request-build time), so ``last_head_role`` defaults to "user" and
+        # the summary is emitted as role="assistant". On a session whose only
+        # genuine user turn falls into the compressed middle — e.g. a
+        # ``hermes kanban`` worker seeded with a single short
+        # ``"work kanban task <id>"`` prompt followed by nothing but
+        # assistant/tool turns — that leaves the compressed transcript with
+        # ZERO user-role messages. OpenAI-compatible backends (vLLM/Qwen)
+        # reject such a request with a non-retryable
+        # ``400 No user query found in messages``, crashing the worker with no
+        # possible recovery (every resume replays the same poisoned history).
+        # If no user-role message survives in either the protected head or the
+        # preserved tail, the summary MUST carry role="user" so the request
+        # always has at least one user turn.
+        if not _force_user_leading:
+            _user_survives = any(
+                messages[i].get("role") == "user"
+                for i in range(0, compress_start)
+            ) or any(
+                messages[i].get("role") == "user"
+                for i in range(compress_end, n_messages)
+            )
+            if not _user_survives:
+                _force_user_leading = True
         # Pick a role that avoids consecutive same-role with both neighbors.
         # Priority: avoid colliding with head (already committed), then tail.
         if last_head_role in {"assistant", "tool"} or _force_user_leading:
diff --git a/tests/agent/test_compressor_zero_user_guard.py b/tests/agent/test_compressor_zero_user_guard.py
new file mode 100644
index 00000000000..e5e3c59286f
--- /dev/null
+++ b/tests/agent/test_compressor_zero_user_guard.py
@@ -0,0 +1,180 @@
+"""Regression coverage for #58753 — compression could drop the only
+user-role message, leaving a transcript with ZERO user turns.
+
+The compressor already pins the handoff summary to ``role="user"`` when
+the only protected head message is the system prompt (#52160). But that
+guard keys off ``last_head_role == "system"``, which is only true when
+the system prompt actually sits inside ``messages`` — the gateway
+``/compress`` path. The main auto-compression path passes the transcript
+WITHOUT the system prompt (it is prepended at request-build time, see
+``conversation_loop`` — ``api_messages = [{"role": "system", ...}] +
+api_messages``). There ``last_head_role`` defaults to ``"user"`` and the
+summary is emitted as ``role="assistant"``.
+
+On a session whose only genuine user turn falls into the compressed
+middle — the canonical shape being a ``hermes kanban`` worker seeded with
+a single short ``"work kanban task <id>"`` prompt followed by nothing but
+assistant/tool turns — the compressed output then contains no user-role
+message at all. OpenAI-compatible backends (vLLM/Qwen) reject such a
+request with a non-retryable ``400 No user query found in messages``,
+crashing the worker with no possible recovery (every resume replays the
+same poisoned history).
+
+The fix generalises the #52160 guard: when NO user-role message survives
+in the protected head or preserved tail, the summary MUST carry
+``role="user"``.
+"""
+
+from __future__ import annotations
+
+from unittest.mock import patch
+
+import pytest
+
+
+@pytest.fixture()
+def compressor():
+    from agent.context_compressor import ContextCompressor
+
+    with patch(
+        "agent.context_compressor.get_model_context_length",
+        return_value=100_000,
+    ):
+        c = ContextCompressor(
+            model="test/model",
+            threshold_percent=0.50,
+            protect_first_n=3,
+            protect_last_n=20,
+            quiet_mode=True,
+        )
+        c.tail_token_budget = 40
+        return c
+
+
+def _tool_turns(start: int, n: int) -> list[dict]:
+    out: list[dict] = []
+    for i in range(start, start + n):
+        out.append(
+            {
+                "role": "assistant",
+                "content": None,
+                "tool_calls": [
+                    {
+                        "id": f"c{i}",
+                        "function": {"name": "read_task", "arguments": "{}"},
+                    }
+                ],
+            }
+        )
+        out.append({"role": "tool", "content": "x" * 300, "tool_call_id": f"c{i}"})
+    return out
+
+
+def _role_hist(messages: list[dict]) -> dict[str, int]:
+    hist: dict[str, int] = {}
+    for m in messages:
+        hist[m.get("role")] = hist.get(m.get("role"), 0) + 1
+    return hist
+
+
+class TestCompressAlwaysKeepsAUserTurn:
+    def test_kanban_worker_recompaction_keeps_user_turn(self, compressor):
+        """The exact #58753 shape: no system prompt in the list, a
+        re-compaction (``protect_first_n`` decayed to 0), and the only
+        user turn old enough to fall into the compressed middle. Before
+        the fix, the summary was emitted as ``assistant`` and the output
+        had zero user-role messages."""
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        # A prior compaction has already happened → protect_first_n decays
+        # to 0 so compress_start lands at 0 (no protected head).
+        c.compression_count = 1
+        # No system message: the main loop prepends it separately.
+        messages = [{"role": "user", "content": "work kanban task 42"}]
+        messages += _tool_turns(0, 12)
+
+        mocked = f"{SUMMARY_PREFIX}\nrolled-up summary of the tool work"
+        with patch.object(c, "_generate_summary", return_value=mocked):
+            out = c.compress(messages, current_tokens=90_000)
+
+        hist = _role_hist(out)
+        assert hist.get("user", 0) >= 1, (
+            "REGRESSION (#58753): compression produced a transcript with "
+            f"zero user-role messages, which vLLM/Qwen reject with a "
+            f"non-retryable 400. Role histogram: {hist}"
+        )
+
+    def test_summary_pinned_to_user_when_no_user_survives(self, compressor):
+        """When the whole compressible region is assistant/tool and no
+        user message survives in head or tail, the inserted summary
+        itself must be the user turn."""
+        from agent.context_compressor import (
+            SUMMARY_PREFIX,
+            COMPRESSED_SUMMARY_METADATA_KEY,
+        )
+
+        c = compressor
+        c.compression_count = 1
+        messages = [{"role": "user", "content": "work kanban task 7"}]
+        messages += _tool_turns(0, 12)
+
+        mocked = f"{SUMMARY_PREFIX}\nsummary body"
+        with patch.object(c, "_generate_summary", return_value=mocked):
+            out = c.compress(messages, current_tokens=90_000)
+
+        summary_rows = [m for m in out if m.get(COMPRESSED_SUMMARY_METADATA_KEY)]
+        assert len(summary_rows) == 1
+        assert summary_rows[0].get("role") == "user", (
+            "The handoff summary must carry role=user when it is the only "
+            "possible user turn in the compressed transcript (#58753)."
+        )
+
+    def test_no_consecutive_user_roles_introduced(self, compressor):
+        """Forcing the summary to role=user must not create two
+        consecutive user-role messages (strict alternation invariant).
+        When a user survives in the tail we do NOT force, so the pinned
+        summary can never collide with a user-role neighbour."""
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        c.compression_count = 1
+        messages = [{"role": "user", "content": "work kanban task 9"}]
+        messages += _tool_turns(0, 12)
+
+        mocked = f"{SUMMARY_PREFIX}\nsummary body"
+        with patch.object(c, "_generate_summary", return_value=mocked):
+            out = c.compress(messages, current_tokens=90_000)
+
+        for prev, cur in zip(out, out[1:]):
+            assert not (
+                prev.get("role") == "user" and cur.get("role") == "user"
+            ), "compression introduced consecutive user-role messages"
+
+    def test_preserved_tail_user_is_not_overridden(self, compressor):
+        """When a genuine user message survives in the tail, the guard
+        must NOT fire (the summary keeps its alternation-driven role) —
+        the request already has a user turn."""
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        c.compression_count = 1
+        c.tail_token_budget = 10  # tight tail so most turns compress
+        messages = [{"role": "user", "content": "old task"}]
+        messages += _tool_turns(0, 10)
+        # A recent, genuine user turn that will be preserved in the tail.
+        messages += [
+            {"role": "user", "content": "the latest live user question"},
+            {"role": "assistant", "content": "on it"},
+        ]
+
+        mocked = f"{SUMMARY_PREFIX}\nsummary body"
+        with patch.object(c, "_generate_summary", return_value=mocked):
+            out = c.compress(messages, current_tokens=90_000)
+
+        hist = _role_hist(out)
+        assert hist.get("user", 0) >= 1
+        joined = "\n".join(
+            m.get("content") for m in out if isinstance(m.get("content"), str)
+        )
+        assert "the latest live user question" in joined