diff --git a/agent/anthropic_adapter.py b/agent/anthropic_adapter.py
index 3c36ee3b91..68b8ca228d 100644
--- a/agent/anthropic_adapter.py
+++ b/agent/anthropic_adapter.py
@@ -2814,7 +2814,26 @@ def convert_messages_to_anthropic(
                     p.get("cache_control") for p in content if isinstance(p, dict)
                 )
                 if has_cache:
-                    system = [p for p in content if isinstance(p, dict)]
+                    # Copy blocks before coercing so the caller's message
+                    # dicts are never mutated, then replace blank/whitespace
+                    # text with the shared non-whitespace placeholder —
+                    # Anthropic rejects a blank system text block with the
+                    # same HTTP 400 as message blocks ("text content blocks
+                    # must contain non-whitespace text"), and a blank block
+                    # carrying a cache_control breakpoint cannot simply be
+                    # dropped (#70909).
+                    system = []
+                    for p in content:
+                        if not isinstance(p, dict):
+                            continue
+                        if (
+                            p.get("type") == "text"
+                            and isinstance(p.get("text"), str)
+                            and not p["text"].strip()
+                        ):
+                            p = dict(p)
+                            p["text"] = _EMPTY_TEXT_PLACEHOLDER
+                        system.append(p)
                 else:
                     system = "\n".join(
                         p["text"] for p in content if p.get("type") == "text"
diff --git a/tests/agent/test_anthropic_request_blank_block_guard.py b/tests/agent/test_anthropic_request_blank_block_guard.py
new file mode 100644
index 0000000000..e253436911
--- /dev/null
+++ b/tests/agent/test_anthropic_request_blank_block_guard.py
@@ -0,0 +1,108 @@
+"""Regression: the final Anthropic request must carry no blank text block.
+
+`convert_messages_to_anthropic` runs per-message converters that coerce blanks
+they produce, but a blank/whitespace-only text block can be synthesized *after*
+those run — a compression summary message, a role merge, or an upstream message
+whose content arrives pre-shaped as content blocks. Any single blank text block
+makes Anthropic reject the whole request with HTTP 400 "text content blocks must
+contain non-whitespace text", which then replays on every turn and wedges the
+session.
+
+`_scrub_blank_text_blocks` is the final backstop on the fully-assembled message
+list, and the system-block path coerces blanks at extraction time (a blank block
+carrying a cache_control breakpoint cannot be dropped).
+Ref #69512 / #70909 (follow-up: request-level guard, not just per-message).
+"""
+from agent.anthropic_adapter import (
+    _EMPTY_TEXT_PLACEHOLDER,
+    convert_messages_to_anthropic,
+)
+
+
+def _all_text_blocks(messages):
+    for m in messages:
+        content = m.get("content")
+        if isinstance(content, list):
+            for b in content:
+                if isinstance(b, dict) and b.get("type") == "text":
+                    yield b
+
+
+def _assert_no_blank(system, messages):
+    if isinstance(system, list):
+        for b in system:
+            if isinstance(b, dict) and b.get("type") == "text":
+                assert b["text"].strip(), f"blank text block in system: {b!r}"
+    for b in _all_text_blocks(messages):
+        assert b["text"].strip(), f"blank text block survived: {b!r}"
+
+
+def test_pre_shaped_blank_block_in_user_content_is_coerced():
+    # Content arrives already as blocks with a blank text part — the per-message
+    # user converter does not walk-and-coerce these, so the final guard must.
+    messages = [
+        {"role": "user", "content": [
+            {"type": "text", "text": "   "},
+            {"type": "text", "text": "real question"},
+        ]},
+    ]
+    system, result = convert_messages_to_anthropic(messages)
+    _assert_no_blank(system, result)
+
+
+def test_blank_summary_style_user_message_is_coerced():
+    # A compression summary that came back empty becomes a whitespace user
+    # message; it must not reach the wire as a blank block.
+    messages = [
+        {"role": "user", "content": "hi"},
+        {"role": "assistant", "content": "answer"},
+        {"role": "user", "content": "\n\n"},  # empty "summary"-style turn
+    ]
+    system, result = convert_messages_to_anthropic(messages)
+    _assert_no_blank(system, result)
+
+
+def test_blank_system_block_is_coerced():
+    messages = [
+        {"role": "system", "content": [
+            {"type": "text", "text": "  ", "cache_control": {"type": "ephemeral"}},
+        ]},
+        {"role": "user", "content": "hello"},
+    ]
+    system, result = convert_messages_to_anthropic(messages)
+    _assert_no_blank(system, result)
+
+
+def test_prepended_leading_user_turn_is_not_blank():
+    """The root cause: _ensure_leading_user_turn prepends a placeholder turn when
+    messages[0] is not a user turn (post-compaction histories start with an
+    assistant summary). That placeholder must be NON-whitespace — a bare " "
+    is itself a blank text block and 400s the whole request, wedging every turn.
+    Bedrock's equivalent already uses the shared placeholder.
+    """
+    messages = [
+        {"role": "assistant", "content": "summary of earlier turns"},
+        {"role": "user", "content": "continue"},
+    ]
+    system, result = convert_messages_to_anthropic(messages)
+    assert result[0]["role"] == "user", "a leading user turn must be prepended"
+    _assert_no_blank(system, result)
+
+
+def test_real_text_is_left_untouched():
+    # A real, non-blank turn keeps its text verbatim and is never replaced by
+    # the placeholder (the guard only touches blank blocks).
+    messages = [
+        {"role": "user", "content": "what is 2+2?"},
+    ]
+    system, result = convert_messages_to_anthropic(messages)
+    # Content may be a plain string or a list of blocks; collect text either way.
+    texts = []
+    for m in result:
+        c = m.get("content")
+        if isinstance(c, str):
+            texts.append(c)
+        elif isinstance(c, list):
+            texts.extend(b.get("text", "") for b in c if isinstance(b, dict) and b.get("type") == "text")
+    assert "what is 2+2?" in texts
+    assert _EMPTY_TEXT_PLACEHOLDER not in texts