diff --git a/src/proxy/transformers/request-transformer.ts b/src/proxy/transformers/request-transformer.ts
index 9083c1da..a87c4dff 100644
--- a/src/proxy/transformers/request-transformer.ts
+++ b/src/proxy/transformers/request-transformer.ts
@@ -671,6 +671,49 @@ function transformMessages(messagesValue: unknown): OpenAIMessage[] {
   return translatedMessages;
 }
 
+/**
+ * Hoist every `role: "system"` message to a single leading system message.
+ *
+ * Claude Code sends the system prompt as the top-level `system` field *and*,
+ * separately, sends skill/plugin listings as `role: "system"` entries inside
+ * `messages` (see #1459). `ProxyRequestTransformer.transform` prepends the
+ * top-level `system` field unconditionally, so once both are present the
+ * resulting array holds two `system` messages that are not adjacent —
+ * `coalesceMessages` only merges *consecutive* same-role messages, so it
+ * cannot fix this case even if it did coalesce `system` (which it explicitly
+ * excludes below).
+ *
+ * Strict OpenAI-compatible backends (LiteLLM among them) reject any request
+ * where a `system` message is not alone at index 0:
+ * `400 A 'system' message can only appear at index 0 of the messages array.`
+ *
+ * This pass extracts all `system` messages in encounter order, joins their
+ * content with a blank line, and reinserts the result as the sole leading
+ * message — content-preserving, order-preserving for everything else.
+ */
+function hoistSystemMessages(messages: OpenAIMessage[]): OpenAIMessage[] {
+  const systemParts: string[] = [];
+  const rest: OpenAIMessage[] = [];
+
+  for (const message of messages) {
+    if (message.role !== 'system') {
+      rest.push(message);
+      continue;
+    }
+    const content = message.content;
+    const text = typeof content === 'string' ? content : '';
+    if (text.trim().length > 0) {
+      systemParts.push(text);
+    }
+  }
+
+  if (systemParts.length === 0) {
+    return rest;
+  }
+
+  return [{ role: 'system', content: systemParts.join('\n\n') }, ...rest];
+}
+
 /**
  * Coalesce consecutive messages of the same role.
  * OpenAI/vLLM/Ollama/Mistral require strict user<->assistant alternation.
@@ -741,7 +784,7 @@ export class ProxyRequestTransformer {
       // was billed. See:
       // https://platform.openai.com/docs/api-reference/chat-streaming
       ...(source.stream === true ? { stream_options: { include_usage: true } } : {}),
-      messages: coalesceMessages(allMessages),
+      messages: coalesceMessages(hoistSystemMessages(allMessages)),
       max_tokens: asNumber(source.max_tokens),
       temperature: asNumber(source.temperature),
       top_p: asNumber(source.top_p),
diff --git a/tests/unit/proxy/transformers/request-transformer-regressions.test.ts b/tests/unit/proxy/transformers/request-transformer-regressions.test.ts
index 656c4e7a..bbeffec3 100644
--- a/tests/unit/proxy/transformers/request-transformer-regressions.test.ts
+++ b/tests/unit/proxy/transformers/request-transformer-regressions.test.ts
@@ -321,4 +321,32 @@ describe('ProxyRequestTransformer regressions', () => {
 
     expect(result.tool_choice).toBe('auto');
   });
+
+  it('merges the top-level system field with a mid-array system message into one leading system message', () => {
+    // Claude Code sends the main system prompt via the top-level `system`
+    // field AND a skill/plugin listing as a `role: "system"` message inside
+    // `messages` (see #1459). Prepending the top-level field unconditionally
+    // used to leave two non-adjacent `system` messages in the payload, which
+    // strict OpenAI-compatible backends (LiteLLM among them) reject with:
+    // `400 A 'system' message can only appear at index 0 of the messages array.`
+    const result = new ProxyRequestTransformer().transform({
+      system: [{ type: 'text', text: 'You are Claude Code, a CLI tool.' }],
+      messages: [
+        {
+          role: 'system',
+          content: 'The following skills are available for use with the Skill tool:\n- foo',
+        },
+        { role: 'user', content: 'ping' },
+      ],
+    });
+
+    const systemMessages = result.messages.filter((message) => message.role === 'system');
+    expect(systemMessages).toHaveLength(1);
+    expect(result.messages[0]).toEqual({
+      role: 'system',
+      content:
+        'You are Claude Code, a CLI tool.\n\nThe following skills are available for use with the Skill tool:\n- foo',
+    });
+    expect(result.messages[1]).toEqual({ role: 'user', content: 'ping' });
+  });
 });
diff --git a/tests/unit/proxy/transformers/request-transformer.test.ts b/tests/unit/proxy/transformers/request-transformer.test.ts
index f3258f07..847f58ba 100644
--- a/tests/unit/proxy/transformers/request-transformer.test.ts
+++ b/tests/unit/proxy/transformers/request-transformer.test.ts
@@ -43,7 +43,7 @@ describe('ProxyRequestTransformer', () => {
     });
   });
 
-  it('accepts Claude Code system messages in the messages array', () => {
+  it('accepts Claude Code system messages in the messages array and hoists them to a single leading system message', () => {
     const transformer = new ProxyRequestTransformer();
     const result = transformer.transform({
       messages: [
@@ -53,10 +53,14 @@ describe('ProxyRequestTransformer', () => {
       ],
     });
 
+    // Strict OpenAI-compatible backends (e.g. LiteLLM) reject any payload
+    // where `system` is not alone at index 0, so a mid-array `system`
+    // message must be hoisted rather than left in place. See #1459 for why
+    // the message must be accepted at all, and the coalesce-duplicate-system
+    // fix for why it can't simply stay where it landed.
     expect(result.messages).toEqual([
-      { role: 'user', content: 'hello' },
       { role: 'system', content: 'answer tersely' },
-      { role: 'user', content: 'which model is this?' },
+      { role: 'user', content: 'hello\nwhich model is this?' },
     ]);
   });