diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index 12c80a8bfb71..dd05ce1e4795 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -857,10 +857,19 @@ def run_conversation(
 
         if moa_config:
             try:
+                from agent.message_content import flatten_message_text as _flatten_mt
                 from agent.moa_loop import _preset_temperature, aggregate_moa_context
 
                 _moa_context = aggregate_moa_context(
-                    user_prompt=original_user_message if isinstance(original_user_message, str) else str(original_user_message),
+                    user_prompt=(
+                        original_user_message
+                        if isinstance(original_user_message, str)
+                        # Multimodal / decorated content list: extract the
+                        # visible text instead of str()-ing a Python repr of
+                        # the parts (which would leak base64 image payloads
+                        # into the aggregator prompt).
+                        else _flatten_mt(original_user_message)
+                    ),
                     api_messages=api_messages,
                     reference_models=moa_config.get("reference_models") or [],
                     aggregator=moa_config.get("aggregator") or {},
@@ -874,6 +883,14 @@ def run_conversation(
                             _base = _msg.get("content", "")
                             if isinstance(_base, str):
                                 _msg["content"] = _base + "\n\n" + _moa_context
+                            elif isinstance(_base, list):
+                                # Multimodal user turn (text + image parts):
+                                # append the MoA context as a trailing text
+                                # part instead of silently dropping it.
+                                _msg["content"] = [
+                                    *_base,
+                                    {"type": "text", "text": "\n\n" + _moa_context},
+                                ]
                             break
             except Exception as _moa_exc:
                 logger.warning("MoA context aggregation failed: %s", _moa_exc)
diff --git a/agent/moa_loop.py b/agent/moa_loop.py
index cd7fa3ea4ea2..267f33dd7e5a 100644
--- a/agent/moa_loop.py
+++ b/agent/moa_loop.py
@@ -14,6 +14,7 @@ from concurrent.futures import ThreadPoolExecutor
 from typing import Any
 
 from agent.auxiliary_client import call_llm
+from agent.message_content import flatten_message_text
 from agent.transports import get_transport
 
 logger = logging.getLogger(__name__)
@@ -470,11 +471,36 @@ def _reference_messages(messages: list[dict[str, Any]]) -> list[dict[str, Any]]:
     for msg in messages:
         role = msg.get("role")
         content = msg.get("content")
-        text = content if isinstance(content, str) else ""
+        # Flatten structured content (lists of parts) to visible text. Content
+        # arrives as a list — not a string — in two common cases:
+        #   1. Anthropic prompt-cache decoration: conversation_loop runs
+        #      apply_anthropic_cache_control BEFORE the MoA facade, converting
+        #      string content to [{"type": "text", "text": ..., "cache_control":
+        #      ...}]. A str-only read here flattened the user's ENTIRE prompt to
+        #      "" — Claude references then 400'd ("messages: at least one
+        #      message is required") while tolerant models answered "no user
+        #      request is present".
+        #   2. Multimodal turns (pasted image → text + image_url parts) and
+        #      multimodal tool results (screenshots).
+        # flatten_message_text extracts the text parts and skips image parts,
+        # and returns strings unchanged — so a decorated and an undecorated
+        # transcript produce a byte-identical advisory view (which keeps the
+        # advisory prefix stable across iterations for advisor prompt caching).
+        text = flatten_message_text(content)
 
         if role == "system":
             continue
         if role == "user":
+            if not text.strip() and content not in (None, "", []):
+                # Structured content with no extractable text (e.g. an
+                # image-only turn). Emitting an empty user message would be
+                # dropped/rejected by strict providers (Anthropic 400s on
+                # empty text blocks — the original "closed" preset failure
+                # mode), and silently skipping the turn would break
+                # user/assistant alternation in the advisory view. Substitute
+                # a placeholder so the reference knows a non-text turn
+                # happened.
+                text = "[user sent non-text content (e.g. an image attachment)]"
             if text.strip():
                 last_user_content = text
             rendered.append({"role": "user", "content": text})
@@ -517,8 +543,10 @@ def _reference_messages(messages: list[dict[str, Any]]) -> list[dict[str, Any]]:
         if last_user_content is not None:
             return [{"role": "user", "content": last_user_content}]
         for msg in reversed(messages):
-            if msg.get("role") == "user" and isinstance(msg.get("content"), str):
-                return [{"role": "user", "content": msg["content"]}]
+            if msg.get("role") == "user":
+                fallback_text = flatten_message_text(msg.get("content"))
+                if fallback_text.strip():
+                    return [{"role": "user", "content": fallback_text}]
     return rendered
 
 
@@ -671,13 +699,28 @@ def _attach_reference_guidance(agg_messages: list[dict[str, Any]], guidance: str
     Appending at the very end keeps the ``[system][task][tool-history]`` prefix
     stable and cache-reusable (only the new block re-prefills), and gives the
     aggregator the references with recency. Merge into the last message only when
-    it is already a trailing string ``user`` turn (plain chat — still at the end).
+    it is already a trailing ``user`` turn (plain chat — still at the end).
+
+    A trailing user turn's content may be a STRING or a LIST of content parts —
+    Anthropic prompt-cache decoration (which runs before the MoA facade)
+    converts string content to ``[{"type": "text", ..., "cache_control": ...}]``,
+    and multimodal turns are lists natively. Both shapes are merged in place:
+    appending a new text part AFTER the cache_control-marked part keeps the
+    cached prefix byte-stable (the marker still terminates it) while the
+    turn-varying guidance rides outside the cached span. Appending a SEPARATE
+    user message here instead would produce two consecutive user turns —
+    strict providers reject that.
     """
     last = agg_messages[-1] if agg_messages else None
-    if last is not None and last.get("role") == "user" and isinstance(last.get("content"), str):
-        last["content"] = last["content"] + "\n\n" + guidance
-    else:
-        agg_messages.append({"role": "user", "content": guidance})
+    if last is not None and last.get("role") == "user":
+        last_content = last.get("content")
+        if isinstance(last_content, str):
+            last["content"] = last_content + "\n\n" + guidance
+            return
+        if isinstance(last_content, list):
+            last["content"] = [*last_content, {"type": "text", "text": "\n\n" + guidance}]
+            return
+    agg_messages.append({"role": "user", "content": guidance})
 
 
 class MoAChatCompletions:
diff --git a/tests/run_agent/test_moa_loop_mode.py b/tests/run_agent/test_moa_loop_mode.py
index 04c7d51ceb10..094278541762 100644
--- a/tests/run_agent/test_moa_loop_mode.py
+++ b/tests/run_agent/test_moa_loop_mode.py
@@ -1059,3 +1059,147 @@ def test_reference_guidance_merges_into_trailing_user_in_plain_chat():
     assert len(messages) == 2
     assert messages[-1]["role"] == "user"
     assert messages[-1]["content"] == "hello\n\nREFERENCE BLOCK"
+
+
+def test_reference_messages_flattens_cache_decorated_content():
+    """Cache-decorated turns (content-part lists) must not blind the references.
+
+    conversation_loop runs apply_anthropic_cache_control BEFORE the MoA facade
+    when the preset's aggregator is a cache-honoring Claude route (post-#57675).
+    That converts string content into [{"type": "text", "text": ...,
+    "cache_control": ...}] lists. The advisory view previously read only string
+    content, so the user's ENTIRE prompt flattened to "" — Claude references
+    then 400'd ("messages: at least one message is required") while tolerant
+    models answered "no user request is present" (live incident, Jul 14 2026,
+    preset "closed", session 20260714_001520_28157b).
+    """
+    from agent.moa_loop import _reference_messages
+    from agent.prompt_caching import apply_anthropic_cache_control
+
+    plain = [
+        {"role": "system", "content": "hermes system prompt"},
+        {"role": "user", "content": "Can we get codex usage resets into hermes?"},
+    ]
+    decorated = apply_anthropic_cache_control(plain, native_anthropic=False)
+    # Premise: decoration really converts the user turn to a content-part list.
+    assert isinstance(decorated[1]["content"], list)
+
+    view = _reference_messages(decorated)
+
+    assert view == [
+        {"role": "user", "content": "Can we get codex usage resets into hermes?"}
+    ]
+    # Invariant: decorated and undecorated transcripts produce the SAME
+    # advisory view — so decoration can never change what references see,
+    # and the advisory prefix stays byte-stable for advisor prompt caching.
+    assert view == _reference_messages(plain)
+
+
+def test_reference_messages_flattens_multimodal_user_turn():
+    """Multimodal user turns (text + image parts) keep their text in the view.
+
+    Image parts carry no advisory text and are skipped; the text part must
+    survive. Previously the whole turn flattened to "".
+    """
+    from agent.moa_loop import _reference_messages
+
+    messages = [
+        {"role": "user", "content": [
+            {"type": "text", "text": "what is in this screenshot?"},
+            {"type": "image_url", "image_url": {"url": "data:image/png;base64,AAAA"}},
+        ]},
+    ]
+
+    view = _reference_messages(messages)
+
+    assert view == [{"role": "user", "content": "what is in this screenshot?"}]
+    # No base64 payload leaks into the advisory view.
+    assert all("base64" not in m["content"] for m in view)
+
+
+def test_reference_messages_image_only_user_turn_gets_placeholder():
+    """An image-only user turn must not become an empty user message.
+
+    Anthropic rejects empty text blocks (the original 400 class) and silently
+    skipping the turn would misalign user/assistant alternation in the view —
+    so a placeholder stands in for the non-text content.
+    """
+    from agent.moa_loop import _reference_messages
+
+    messages = [
+        {"role": "user", "content": [
+            {"type": "image_url", "image_url": {"url": "data:image/png;base64,AAAA"}},
+        ]},
+        {"role": "assistant", "content": "I see a diagram."},
+        {"role": "user", "content": "now explain it"},
+    ]
+
+    view = _reference_messages(messages)
+
+    assert view[0]["role"] == "user"
+    assert view[0]["content"].strip(), "image-only turn must not be empty"
+    assert "non-text" in view[0]["content"]
+    assert view[-1] == {"role": "user", "content": "now explain it"}
+
+
+def test_reference_messages_flattens_structured_assistant_and_tool_content():
+    """Assistant and tool turns with content-part lists are flattened too.
+
+    Multimodal tool results (e.g. computer_use screenshots) and adapter-shaped
+    assistant turns arrive as lists; their text must reach the references and
+    their image parts must not leak.
+    """
+    from agent.moa_loop import _reference_messages
+
+    messages = [
+        {"role": "user", "content": "check the screen"},
+        {
+            "role": "assistant",
+            "content": [{"type": "text", "text": "taking a screenshot"}],
+            "tool_calls": [{"id": "c1", "function": {"name": "capture", "arguments": "{}"}}],
+        },
+        {"role": "tool", "tool_call_id": "c1", "content": [
+            {"type": "text", "text": "screenshot captured: login page visible"},
+            {"type": "image_url", "image_url": {"url": "data:image/png;base64,BBBB"}},
+        ]},
+    ]
+
+    view = _reference_messages(messages)
+
+    joined = "\n".join(m["content"] for m in view)
+    assert "taking a screenshot" in joined
+    assert "[called tool: capture(" in joined
+    assert "[tool result: screenshot captured: login page visible]" in joined
+    assert "BBBB" not in joined
+    assert view[-1]["role"] == "user"
+
+
+def test_reference_guidance_appends_text_part_to_decorated_trailing_user():
+    """A cache-decorated trailing user turn still receives the guidance block.
+
+    Decoration converts the trailing user turn to a content-part list; the
+    guidance must be appended as a NEW text part AFTER the cache_control-marked
+    part (cached prefix stays byte-stable, no consecutive-user-turn 400s), not
+    silently dropped and not added as a second user message.
+    """
+    from agent.moa_loop import _attach_reference_guidance
+
+    marked_part = {
+        "type": "text",
+        "text": "hello",
+        "cache_control": {"type": "ephemeral"},
+    }
+    messages = [
+        {"role": "system", "content": "system prompt"},
+        {"role": "user", "content": [dict(marked_part)]},
+    ]
+    _attach_reference_guidance(messages, "REFERENCE BLOCK")
+
+    # No extra message (would break user/user alternation).
+    assert len(messages) == 2
+    content = messages[-1]["content"]
+    assert isinstance(content, list) and len(content) == 2
+    # The cache-marked part is byte-identical (prefix stability).
+    assert content[0] == marked_part
+    # The guidance rides as a trailing text part outside the cached span.
+    assert content[1] == {"type": "text", "text": "\n\nREFERENCE BLOCK"}