diff --git a/agent/conversation_compression.py b/agent/conversation_compression.py
index 37b681b3a75..723f50d2ea0 100644
--- a/agent/conversation_compression.py
+++ b/agent/conversation_compression.py
@@ -1969,6 +1969,21 @@ def compress_context(
         ):
             new_system_prompt = cached_system_prompt
             agent._cached_system_prompt = cached_system_prompt
+            # _invalidate_system_prompt() above also cleared the
+            # cross-session-stable prefix marker boundary. The kept prompt
+            # is byte-identical, so reconstruct the stable tier and reuse
+            # it ONLY when the kept prompt still literally starts with it
+            # (same startswith gate as the restore path); otherwise the
+            # request layer falls back to the legacy single-breakpoint
+            # layout with the prompt bytes untouched.
+            try:
+                from agent.system_prompt import build_system_prompt_parts as _build_parts
+
+                _static = _build_parts(agent, system_message=system_message)["stable"]
+                if _static and cached_system_prompt.startswith(_static):
+                    agent._cached_system_prompt_static = _static
+            except Exception:
+                pass
         else:
             new_system_prompt = agent._build_system_prompt(system_message)
             agent._cached_system_prompt = new_system_prompt
diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index daa6cac807a..fae6ff2e695 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -436,6 +436,37 @@ def _restore_or_build_system_prompt(agent, system_message, conversation_history)
         # Continuing session — reuse the exact system prompt from the
         # previous turn so the Anthropic cache prefix matches.
         agent._cached_system_prompt = stored_prompt
+        # Reconstruct the cross-session-stable prefix for the early cache
+        # breakpoint. The static prefix is not persisted (only the full
+        # prompt is), so gateway surfaces that build a fresh AIAgent per
+        # turn would otherwise lose the two-block system layout after the
+        # first turn — flip-flopping the wire shape mid-conversation and
+        # silently degrading to the legacy single-breakpoint layout.
+        #
+        # Safety: the rebuilt stable tier is used ONLY when the restored
+        # prompt literally starts with it (checked here AND re-checked by
+        # ``_apply_system_cache_markers``'s ``startswith`` gate). If any
+        # stable-tier input changed since the prompt was persisted (skills
+        # edited, identity changed), the prefix mismatches, ``_static``
+        # stays None, and the request falls back to the legacy layout with
+        # the restored prompt bytes untouched — never a rewritten prompt.
+        #
+        # Gated on ``_use_prompt_caching`` so non-Anthropic routes skip the
+        # rebuild entirely (the static prefix is only consumed by
+        # ``apply_anthropic_cache_control``).
+        if getattr(agent, "_use_prompt_caching", False):
+            try:
+                from agent.system_prompt import build_system_prompt_parts as _build_parts
+
+                _static = _build_parts(agent, system_message=system_message)["stable"]
+                if _static and stored_prompt.startswith(_static):
+                    agent._cached_system_prompt_static = _static
+            except Exception:
+                # Fail-open: restore continues with the legacy cache layout.
+                logger.debug(
+                    "static system-prefix reconstruction failed on restore",
+                    exc_info=True,
+                )
         return
     if stored_prompt:
         stored_state = "stale_runtime"
diff --git a/tests/agent/test_system_prompt_restore.py b/tests/agent/test_system_prompt_restore.py
index 956c1152a42..72564325d93 100644
--- a/tests/agent/test_system_prompt_restore.py
+++ b/tests/agent/test_system_prompt_restore.py
@@ -32,6 +32,10 @@ def _make_agent(session_db=None, prebuilt_prompt: str = "BUILT_PROMPT"):
     agent.provider = "openrouter"
     agent.platform = "cli"
     agent._session_db = session_db
+    # MagicMock attributes are truthy by default; the static-prefix
+    # reconstruction is gated on _use_prompt_caching, so default it off
+    # for the legacy restore tests (the reconstruction tests enable it).
+    agent._use_prompt_caching = False
     agent._build_system_prompt = MagicMock(return_value=prebuilt_prompt)
     return agent
 
@@ -261,5 +265,90 @@ class TestPromptStabilityInvariant:
         assert agent._cached_system_prompt.encode("utf-8") == stored.encode("utf-8")
 
 
+# ---------------------------------------------------------------------------
+# Cross-session static prefix reconstruction (issue #68191 follow-up)
+# ---------------------------------------------------------------------------
+
+
+class TestStaticPrefixReconstructionOnRestore:
+    """The two-block cache layout must survive session restore.
+
+    Gateway surfaces construct a fresh AIAgent per turn and restore the
+    persisted prompt from the session DB; the cross-session-stable prefix
+    (``_cached_system_prompt_static``) is only set on fresh builds, so
+    without reconstruction the wire layout silently degrades to the legacy
+    single-breakpoint layout after turn 1 (flagged on PR #68258 review).
+    """
+
+    def test_restore_reconstructs_static_prefix_when_it_matches(self):
+        stable = "STATIC IDENTITY AND GUIDANCE"
+        stored = stable + "\n\nper-session context\n\nvolatile tail"
+        db = MagicMock()
+        db.get_session.return_value = {"system_prompt": stored}
+        agent = _make_agent(session_db=db)
+        agent._use_prompt_caching = True
+        agent._cached_system_prompt_static = None
+
+        from unittest.mock import patch as _patch
+
+        with _patch(
+            "agent.system_prompt.build_system_prompt_parts",
+            return_value={"stable": stable, "context": "", "volatile": ""},
+        ):
+            _restore_or_build_system_prompt(
+                agent, None, [{"role": "user", "content": "hi"}]
+            )
+
+        # Restored prompt bytes untouched; static prefix reconstructed.
+        assert agent._cached_system_prompt == stored
+        assert agent._cached_system_prompt_static == stable
+
+    def test_restore_leaves_static_unset_on_prefix_mismatch(self):
+        """Stable-tier drift (skills edited since persist) → no static prefix,
+        legacy layout, restored bytes still authoritative."""
+        stored = "OLD STATIC HEAD\n\nper-session context"
+        db = MagicMock()
+        db.get_session.return_value = {"system_prompt": stored}
+        agent = _make_agent(session_db=db)
+        agent._use_prompt_caching = True
+        agent._cached_system_prompt_static = None
+
+        from unittest.mock import patch as _patch
+
+        with _patch(
+            "agent.system_prompt.build_system_prompt_parts",
+            return_value={"stable": "NEW STATIC HEAD", "context": "", "volatile": ""},
+        ):
+            _restore_or_build_system_prompt(
+                agent, None, [{"role": "user", "content": "hi"}]
+            )
+
+        assert agent._cached_system_prompt == stored
+        assert agent._cached_system_prompt_static is None
+
+    def test_restore_survives_parts_builder_exception(self):
+        """Prefix reconstruction is fail-open: a parts-builder crash must not
+        break the byte-identical restore."""
+        stored = "Stored prompt — must survive"
+        db = MagicMock()
+        db.get_session.return_value = {"system_prompt": stored}
+        agent = _make_agent(session_db=db)
+        agent._use_prompt_caching = True
+        agent._cached_system_prompt_static = None
+
+        from unittest.mock import patch as _patch
+
+        with _patch(
+            "agent.system_prompt.build_system_prompt_parts",
+            side_effect=RuntimeError("boom"),
+        ):
+            _restore_or_build_system_prompt(
+                agent, None, [{"role": "user", "content": "hi"}]
+            )
+
+        assert agent._cached_system_prompt == stored
+        assert agent._cached_system_prompt_static is None
+
+
 if __name__ == "__main__":
     pytest.main([__file__, "-v"])