diff --git a/open-sse/handlers/chatCore.ts b/open-sse/handlers/chatCore.ts
index 3c240717ad..7a4af8eb7c 100644
--- a/open-sse/handlers/chatCore.ts
+++ b/open-sse/handlers/chatCore.ts
@@ -9,10 +9,12 @@ import { buildFailureUsageRecord } from "./chatCore/failureUsage.ts";
 import { estimateFinalInputTokens } from "./chatCore/contextEstimation.ts";
 import {
   extractSystemRoleMessages,
+  hoistLeadingTextSystemMessages,
   relocateDirectiveOnlyMessages,
 } from "./chatCore/claudeSystemRole.ts";
 export {
   extractSystemRoleMessages,
+  hoistLeadingTextSystemMessages,
   relocateDirectiveOnlyMessages,
 } from "./chatCore/claudeSystemRole.ts";
 import { checkIdempotencyCache } from "./chatCore/idempotency.ts";
@@ -2312,6 +2314,10 @@ export async function handleChatCore({
           // messages[], but a directive-only message (content: [] +
           // output_config) at messages[0] is rejected by Anthropic. Move it past
           // the first real turn; Anthropic accepts the form at any other position.
+          // A text-bearing system message at messages[0] (e.g. the Output Styles
+          // injection) is rejected there too: hoist the leading run into the
+          // top-level `system` parameter first.
+          hoistLeadingTextSystemMessages(translatedBody);
           relocateDirectiveOnlyMessages(translatedBody);
         }
         if (Array.isArray(translatedBody.messages)) {
diff --git a/open-sse/handlers/chatCore/claudeSystemRole.ts b/open-sse/handlers/chatCore/claudeSystemRole.ts
index 106d521ad0..a84f3f9b72 100644
--- a/open-sse/handlers/chatCore/claudeSystemRole.ts
+++ b/open-sse/handlers/chatCore/claudeSystemRole.ts
@@ -164,6 +164,61 @@ export function extractSystemRoleMessages(payload: Record<string, unknown>): voi
   payload.messages = messages.filter((m) => !isSystemRole(m.role));
 }
 
+/**
+ * Hoists the leading run of text-bearing system-role messages (everything
+ * before the first real user/assistant turn) into the top-level `system`
+ * parameter. Anthropic treats `messages[0]` as the initial system prompt
+ * position and rejects any non-directive system-role message there ("use the
+ * top-level 'system' parameter for the initial system prompt"), which is
+ * exactly where the Output Styles injection lands on the mid-conversation
+ * system passthrough (provider `claude` + 1M-context models). Only the leading
+ * run is hoisted so genuine mid-conversation system turns keep their position
+ * and cache prefix; empty (directive-only) messages in the run are left in
+ * place for relocateDirectiveOnlyMessages to handle.
+ */
+export function hoistLeadingTextSystemMessages(payload: Record<string, unknown>): void {
+  if (!Array.isArray(payload.messages) || payload.messages.length === 0) return;
+  const messages = payload.messages as Array<Record<string, unknown>>;
+  const isSystemRole = (role: unknown): boolean =>
+    typeof role === "string" &&
+    (role.toLowerCase() === "system" || role.toLowerCase() === "developer");
+
+  const blocks: Array<Record<string, unknown>> = [];
+  const kept: Array<Record<string, unknown>> = [];
+  let i = 0;
+  for (; i < messages.length; i++) {
+    const m = messages[i];
+    if (m == null || typeof m !== "object" || !isSystemRole(m.role)) break;
+    if (typeof m.content === "string") {
+      if (m.content.length > 0) blocks.push({ type: "text", text: m.content });
+      continue;
+    }
+    if (Array.isArray(m.content) && m.content.length > 0) {
+      let hoisted = false;
+      for (const block of m.content as Array<Record<string, unknown>>) {
+        if (block?.type === "text" && typeof block.text === "string" && block.text.length > 0) {
+          blocks.push({ type: "text", text: block.text });
+          hoisted = true;
+        }
+      }
+      if (!hoisted) kept.push(m);
+      continue;
+    }
+    kept.push(m);
+  }
+  if (blocks.length === 0) return;
+
+  const existing = payload.system;
+  if (typeof existing === "string" && existing.length > 0) {
+    payload.system = [{ type: "text", text: existing }, ...blocks];
+  } else if (Array.isArray(existing)) {
+    payload.system = [...(existing as Array<Record<string, unknown>>), ...blocks];
+  } else {
+    payload.system = blocks;
+  }
+  payload.messages = [...kept, ...messages.slice(i)];
+}
+
 /**
  * Moves a directive-only system message (empty content array + message-level
  * `output_config`, the shape Claude Code clients emit) off `messages[0]`.
diff --git a/tests/unit/claude-leading-text-system-hoist.test.ts b/tests/unit/claude-leading-text-system-hoist.test.ts
new file mode 100644
index 0000000000..95787bea7c
--- /dev/null
+++ b/tests/unit/claude-leading-text-system-hoist.test.ts
@@ -0,0 +1,77 @@
+import assert from "node:assert/strict";
+import { test } from "node:test";
+
+import {
+  hoistLeadingTextSystemMessages,
+  relocateDirectiveOnlyMessages,
+} from "../../open-sse/handlers/chatCore/claudeSystemRole.ts";
+
+// Reproduction of the production 400 (2026-09-03/04): Output Styles injects a
+// text system message at messages[0]; on the mid-conversation-system passthrough
+// Anthropic rejects it ("use the top-level 'system' parameter for the initial
+// system prompt").
+test("hoistLeadingTextSystemMessages moves a text system messages[0] into top-level system", () => {
+  const payload: Record<string, unknown> = {
+    system: [{ type: "text", text: "You are Claude." }],
+    output_config: { effort: "medium" },
+    messages: [
+      { role: "system", content: "[OmniRoute Output Styles]\nRespond terse." },
+      { role: "user", content: "Reply exactly: MIDCONV_TOPLEVEL_OK" },
+    ],
+  };
+  hoistLeadingTextSystemMessages(payload);
+  assert.deepEqual(payload.system, [
+    { type: "text", text: "You are Claude." },
+    { type: "text", text: "[OmniRoute Output Styles]\nRespond terse." },
+  ]);
+  assert.equal((payload.messages as Array<{ role: string }>)[0].role, "user");
+  assert.equal((payload.messages as unknown[]).length, 1);
+});
+
+test("hoistLeadingTextSystemMessages converts a string top-level system and keeps mid-conversation system turns", () => {
+  const payload: Record<string, unknown> = {
+    system: "base",
+    messages: [
+      { role: "system", content: [{ type: "text", text: "style" }] },
+      { role: "user", content: "hello" },
+      { role: "system", content: "mid-conversation context" },
+      { role: "assistant", content: "hi" },
+    ],
+  };
+  hoistLeadingTextSystemMessages(payload);
+  assert.deepEqual(payload.system, [
+    { type: "text", text: "base" },
+    { type: "text", text: "style" },
+  ]);
+  const roles = (payload.messages as Array<{ role: string }>).map((m) => m.role);
+  assert.deepEqual(roles, ["user", "system", "assistant"]);
+});
+
+test("hoistLeadingTextSystemMessages leaves directive-only messages for relocateDirectiveOnlyMessages", () => {
+  const payload: Record<string, unknown> = {
+    messages: [
+      { role: "system", content: [], output_config: { effort: "high" } },
+      { role: "system", content: "style" },
+      { role: "user", content: "hello" },
+      { role: "assistant", content: "hi" },
+    ],
+  };
+  hoistLeadingTextSystemMessages(payload);
+  assert.deepEqual(payload.system, [{ type: "text", text: "style" }]);
+  relocateDirectiveOnlyMessages(payload);
+  const msgs = payload.messages as Array<Record<string, unknown>>;
+  assert.equal(msgs[0].role, "user");
+  assert.equal(msgs[1].role, "system");
+  assert.deepEqual(msgs[1].output_config, { effort: "high" });
+  assert.equal(msgs[2].role, "assistant");
+});
+
+test("hoistLeadingTextSystemMessages is a no-op for a normal user first message", () => {
+  const payload: Record<string, unknown> = {
+    system: "base",
+    messages: [{ role: "user", content: "hello" }],
+  };
+  hoistLeadingTextSystemMessages(payload);
+  assert.equal(payload.system, "base");
+  assert.equal((payload.messages as unknown[]).length, 1);
+});