diff --git a/agent/prompt_caching.py b/agent/prompt_caching.py
index 719bd58e4afaa..fa8b5ace8447b 100644
--- a/agent/prompt_caching.py
+++ b/agent/prompt_caching.py
@@ -99,12 +99,28 @@ def _apply_system_cache_markers(
     static_system_prefix: str | None,
     *,
     native_anthropic: bool,
+    mark_suffix: bool = True,
+    fallback_to_whole: bool = True,
 ) -> int:
-    """Mark the static system prefix and full prompt when they can be split.
+    """Mark the static system prefix (and optionally the full prompt).
 
     The system prompt remains one stored string. Splitting it only in the
     outgoing request keeps session persistence and non-Anthropic transports
     unchanged while making the stable prefix independently cacheable.
+
+    ``mark_suffix=False`` is the tool-cache-plan layout: only the static
+    prefix carries a marker, the volatile suffix rides unmarked (its
+    breakpoint budget is spent on the tools array instead).
+
+    ``fallback_to_whole=False`` skips marking entirely when the prefix
+    split is not possible (no prefix, mismatched prefix, non-string
+    content) instead of marking the whole message.
+
+    When the prompt IS exactly the static prefix (empty suffix), the whole
+    message is marked as a single block — never a two-part split with an
+    empty text block, which Anthropic rejects.
+
+    Returns the number of markers applied (0, 1, or 2).
     """
     content = message.get("content")
     if (
@@ -115,16 +131,26 @@ def _apply_system_cache_markers(
     ):
         suffix = content[len(static_system_prefix):]
         if suffix:
+            suffix_part: dict = {"type": "text", "text": suffix}
+            if mark_suffix:
+                suffix_part["cache_control"] = cache_marker
             message["content"] = [
                 {
                     "type": "text",
                     "text": static_system_prefix,
                     "cache_control": cache_marker,
                 },
-                {"type": "text", "text": suffix, "cache_control": cache_marker},
+                suffix_part,
             ]
-            return 2
+            return 2 if mark_suffix else 1
+        # Empty suffix: the stored prompt IS the static prefix. Mark it as
+        # one whole block — a [marked-prefix, ""] split would put an empty
+        # text block on the wire (HTTP 400 on native Anthropic).
+        _apply_cache_marker(message, cache_marker, native_anthropic=native_anthropic)
+        return 1
 
+    if not fallback_to_whole:
+        return 0
     _apply_cache_marker(message, cache_marker, native_anthropic=native_anthropic)
     return 1
 
@@ -262,29 +288,6 @@ def _completed_transaction_endpoint_indexes(
     return endpoints
 
 
-def _apply_static_prefix_marker(
-    messages: List[Dict[str, Any]],
-    cache_marker: Dict[str, str],
-    static_system_prefix: str | None,
-) -> None:
-    """Mark only the reusable static system prefix for a tool-cache plan."""
-    if not messages or not isinstance(static_system_prefix, str) or not static_system_prefix:
-        return
-    system = messages[0]
-    if not isinstance(system, dict):
-        return
-    content = system.get("content")
-    if system.get("role") != "system" or not isinstance(content, str):
-        return
-    if not content.startswith(static_system_prefix):
-        return
-    suffix = content[len(static_system_prefix):]
-    system["content"] = [
-        {"type": "text", "text": static_system_prefix, "cache_control": cache_marker},
-        {"type": "text", "text": suffix},
-    ]
-
-
 def build_prompt_cache_plan(
     api_messages: List[Dict[str, Any]],
     tools: List[Dict[str, Any]] | None,
@@ -313,7 +316,21 @@ def build_prompt_cache_plan(
         )
 
     marker = _build_marker(cache_ttl)
-    _apply_static_prefix_marker(messages, marker, static_system_prefix)
+    if (
+        messages
+        and isinstance(messages[0], dict)
+        and messages[0].get("role") == "system"
+    ):
+        # Tool-cache layout: only the static prefix carries a system-side
+        # marker; the volatile suffix's budget is spent on the tools array.
+        _apply_system_cache_markers(
+            messages[0],
+            marker,
+            static_system_prefix,
+            native_anthropic=True,
+            mark_suffix=False,
+            fallback_to_whole=False,
+        )
     planned_tools[-1]["cache_control"] = dict(marker)
     for endpoint in _completed_transaction_endpoint_indexes(
         messages,
diff --git a/tests/agent/test_prompt_caching.py b/tests/agent/test_prompt_caching.py
index d67adffc0b40c..72067935e454b 100644
--- a/tests/agent/test_prompt_caching.py
+++ b/tests/agent/test_prompt_caching.py
@@ -129,6 +129,33 @@ class TestPromptCachePlan:
         assert plan.marker_count == 2
         assert "cache_control" not in plan.messages[-1]
 
+    def test_static_prefix_equal_to_whole_prompt_emits_no_empty_block(self):
+        """Empty volatile suffix must not produce an empty text block.
+
+        Anthropic rejects text blocks whose ``text`` is empty; when the
+        stored system prompt IS the static prefix (no volatile tier), the
+        plan must mark it as one whole block instead of a two-part split
+        with a trailing ``{"type": "text", "text": ""}``.
+        """
+        messages = [
+            {"role": "system", "content": "stable prefix"},
+            {"role": "user", "content": "lookup"},
+        ]
+        plan = build_prompt_cache_plan(
+            messages,
+            _tool_heavy_native_tools(),
+            native_anthropic=True,
+            static_system_prefix="stable prefix",
+            direct_native_tool_cache=True,
+        )
+
+        system_content = plan.messages[0]["content"]
+        assert isinstance(system_content, list)
+        for part in system_content:
+            assert part.get("text"), "no empty text blocks on the wire"
+        assert any("cache_control" in part for part in system_content)
+        assert plan.tools[-1]["cache_control"] == MARKER
+
     def test_tool_strip_is_request_local(self):
         tools = _tool_heavy_native_tools()
         tools[-1]["cache_control"] = MARKER