diff --git a/agent/context_compressor.py b/agent/context_compressor.py
index b4eaec660a4ea..1a24567d13f17 100644
--- a/agent/context_compressor.py
+++ b/agent/context_compressor.py
@@ -6264,16 +6264,18 @@ This compaction should PRIORITISE preserving all information related to the focu
                 None,
             )
         first_tail_role = None
+        first_tail_visible_idx: Optional[int] = None
         if tail_messages:
-            first_tail_role = next(
+            first_tail_visible_idx, first_tail_role = next(
                 (
-                    role
-                    for role in (
-                        _template_visible_role(m) for m in tail_messages
+                    (idx, role)
+                    for idx, role in (
+                        (idx, _template_visible_role(m))
+                        for idx, m in enumerate(tail_messages)
                     )
                     if role is not None
                 ),
-                None,
+                (None, None),
             )
         # When the only protected head message is the system prompt, the
         # summary becomes the first *visible* message in the API request
@@ -6300,11 +6302,27 @@ This compaction should PRIORITISE preserving all information related to the focu
         # 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.
+        #
+        # A bare role check is not enough: the tail's sole surviving user
+        # turn can be image-only (a screenshot with no caption). The newest
+        # image-bearing user message is the ``_strip_historical_media``
+        # anchor and is kept byte-for-byte, so it never gains a text
+        # placeholder — its role is "user" but its text content is empty,
+        # which backends checking for actual query text still reject. Count
+        # only user messages with non-empty text as "surviving"; when the
+        # guard fires, the real (never fabricated) summary text lands in a
+        # role="user" slot, which is always non-empty (falls back to
+        # ``_build_static_fallback_summary`` above when generation fails).
         if not _force_user_leading:
+            def _is_nonempty_user_turn(message: Dict[str, Any]) -> bool:
+                return message.get("role") == "user" and bool(
+                    _content_text_for_contains(message.get("content")).strip()
+                )
+
             _user_survives = any(
-                message.get("role") == "user" for message in compressed
+                _is_nonempty_user_turn(message) for message in compressed
             ) or any(
-                message.get("role") == "user" for message in tail_messages
+                _is_nonempty_user_turn(message) for message in tail_messages
             )
             if not _user_survives:
                 _force_user_leading = True
@@ -6360,9 +6378,27 @@ This compaction should PRIORITISE preserving all information related to the focu
                 ),
             })
 
+        # Default merge target: literal tail index 0. For an ordinary
+        # alternation collision the summary only has to stay *invisible* to
+        # the template, and a leading template-exempt row (bare tool-call
+        # assistant message, tool result) is the ideal carrier — it absorbs
+        # the summary without adding a visible turn, and it leaves the live
+        # tail user message intact as the model's actual prompt. Retargeting
+        # to the first template-visible row here would convert that live
+        # request into the summary carrier for no benefit.
+        #
+        # The forced repair path is the exception. There the merge is not
+        # about alternation but about guaranteeing at least one genuinely
+        # non-empty role="user" message (an image-only or otherwise
+        # text-empty surviving user row). An exempt carrier cannot satisfy
+        # that invariant, so the summary text must land on the
+        # template-visible row itself.
+        _merge_target_idx = 0
+        if _force_user_leading and first_tail_visible_idx is not None:
+            _merge_target_idx = first_tail_visible_idx
         for tail_idx, msg in enumerate(tail_messages):
-            if _merge_summary_into_tail and tail_idx == 0:
-                # Merge the summary into the first (post-strip) tail message.
+            if _merge_summary_into_tail and tail_idx == _merge_target_idx:
+                # Merge the summary into the tail message that collided.
                 old_content = msg.get("content", "")
                 if _force_user_leading and summary_role == "user":
                     # The summary must be part of the first user-visible
diff --git a/tests/agent/test_compressor_zero_user_guard.py b/tests/agent/test_compressor_zero_user_guard.py
index 9cf82c265b444..27973befc9f91 100644
--- a/tests/agent/test_compressor_zero_user_guard.py
+++ b/tests/agent/test_compressor_zero_user_guard.py
@@ -154,3 +154,123 @@ class TestCompressAlwaysKeepsAUserTurn:
             m.get("content") for m in out if isinstance(m.get("content"), str)
         )
         assert "the latest live user question" in joined
+
+
+def _has_nonempty_user_text(messages: list[dict]) -> bool:
+    """True if some role="user" message carries non-empty text.
+
+    Deliberately narrower than "any message has text": a non-empty
+    ``role="assistant"`` summary does not satisfy backends that require an
+    actual user query, so checking role and content together is the point.
+    """
+    from agent.context_compressor import _content_text_for_contains
+
+    return any(
+        m.get("role") == "user"
+        and _content_text_for_contains(m.get("content")).strip()
+        for m in messages
+    )
+
+
+class TestCompressKeepsANonEmptyUserTurn:
+    """A bare ``role == "user"`` check is not enough: the surviving user
+    message can be image-only (no caption). ``_strip_historical_media``
+    anchors on the newest image-bearing user message and keeps it
+    byte-for-byte — it never gains a text placeholder — so a role-only
+    guard is satisfied while the request still has zero *text* user
+    turns, which is what backends actually reject on.
+    """
+
+    def test_image_only_tail_user_turn_still_yields_non_empty_text(self, compressor):
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        c.compression_count = 1
+        # No system message and no protected head (compression_count=1
+        # decays protect_first_n to 0), same #58753 shape — except the
+        # only surviving user turn is an image with no caption text.
+        messages = [{"role": "user", "content": "work kanban task 42"}]
+        messages += _tool_turns(0, 12)
+        messages += [{
+            "role": "user",
+            "content": [
+                {"type": "image_url", "image_url": {"url": "data:image/png;base64,AAAA"}},
+            ],
+        }]
+
+        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
+        assert _has_nonempty_user_text(out), (
+            "REGRESSION: an image-only user turn satisfied the role-only "
+            "zero-user-turn guard, leaving a transcript with a user-role "
+            "message but no actual query text — the exact class of "
+            "request backends reject with 'No user query found in "
+            f"messages'. Output: {out}"
+        )
+
+    def test_image_only_protected_head_still_yields_non_empty_text(self, compressor):
+        """Isolates the ``_user_survives`` text check from the merge-target
+        fix below: here ``compress_start != 0`` and there's no system
+        message, so neither existing force condition
+        (``compress_start == 0`` / ``last_head_role == "system"``) fires on
+        its own — only the broadened (text-aware) survival check does.
+        """
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        c.protect_first_n = 1
+        c.protect_last_n = 2
+        c.tail_token_budget = 10
+        c.compression_count = 0
+
+        messages = [{
+            "role": "user",
+            "content": [
+                {"type": "image_url", "image_url": {"url": "data:image/png;base64,AAAA"}},
+            ],
+        }]
+        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)
+
+        assert _has_nonempty_user_text(out), (
+            "REGRESSION: an image-only protected-head user turn satisfied "
+            f"the role-only zero-user-turn guard. Output: {out}"
+        )
+
+    def test_merge_targets_the_colliding_tail_message_not_index_zero(self, compressor):
+        """Template-exempt rows (bare tool-call assistant / tool messages)
+        ahead of the colliding tail user message must not divert the merge:
+        merging into literal tail index 0 would attach the summary to an
+        exempt row and leave the real (image-only) user message untouched
+        and still empty, silently defeating the forced role="user" this
+        block exists to guarantee.
+        """
+        from agent.context_compressor import SUMMARY_PREFIX
+
+        c = compressor
+        c.compression_count = 1  # decays protect_first_n to 0 -> compress_start == 0
+        messages = [{"role": "user", "content": "work kanban task 42"}]
+        messages += _tool_turns(0, 12)
+        messages += [{
+            "role": "user",
+            "content": [
+                {"type": "image_url", "image_url": {"url": "data:image/png;base64,AAAA"}},
+            ],
+        }]
+
+        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)
+
+        assert _has_nonempty_user_text(out), (
+            "REGRESSION: the summary merged into tail index 0 (a "
+            "template-exempt row) instead of the colliding image-only "
+            f"user message, leaving zero non-empty user turns. Output: {out}"
+        )