diff --git a/core/util/messageConversion.ts b/core/util/messageConversion.ts
index 0712b4d90d5..97c2997137b 100644
--- a/core/util/messageConversion.ts
+++ b/core/util/messageConversion.ts
@@ -355,6 +355,17 @@ export function convertFromUnifiedHistory(
 
 /**
  * Convert ChatHistoryItem array to ChatCompletionMessageParam array with injected system message
+ *
+ * Many OpenAI-compatible providers require the system message to be the very
+ * first message in the array. The history can contain additional system
+ * messages (e.g. notifications added via `addSystemMessage`, compaction notices,
+ * or a system message already stored at `history[0]` in loaded/remote sessions).
+ * If those were emitted inline, the resulting array would have a system message
+ * at a non-zero index and the provider would reject the request with a
+ * "System message must be at the beginning" 400 error (notably surfaced after
+ * cancelling a tool call, which triggers a follow-up request). To avoid this we
+ * merge all system content into a single system message positioned at index 0.
+ *
  * @param historyItems - The chat history items
  * @param systemMessage - The system message to inject at the beginning
  */
@@ -362,17 +373,35 @@ export function convertFromUnifiedHistoryWithSystemMessage(
   historyItems: ChatHistoryItem[],
   systemMessage: string,
 ): ChatCompletionMessageParam[] {
+  const convertedMessages = convertFromUnifiedHistory(historyItems);
+
+  // Collect system content (the injected message plus any system messages that
+  // ended up inside the history) and keep the remaining messages in order.
+  const systemContents: string[] = [];
+  if (systemMessage.trim()) {
+    systemContents.push(systemMessage);
+  }
+
+  const nonSystemMessages: ChatCompletionMessageParam[] = [];
+  for (const message of convertedMessages) {
+    if (message.role === "system") {
+      if (typeof message.content === "string" && message.content.trim()) {
+        systemContents.push(message.content);
+      }
+      continue;
+    }
+    nonSystemMessages.push(message);
+  }
+
   const messages: ChatCompletionMessageParam[] = [];
 
-  // Inject system message at the beginning
+  // Always inject a single system message at the beginning
   messages.push({
     role: "system",
-    content: systemMessage,
+    content: systemContents.join("\n\n"),
   });
 
-  // Convert the rest of the history
-  const convertedMessages = convertFromUnifiedHistory(historyItems);
-  messages.push(...convertedMessages);
+  messages.push(...nonSystemMessages);
 
   return messages;
 }
diff --git a/extensions/cli/src/messageConversion.test.ts b/extensions/cli/src/messageConversion.test.ts
index 45e7de2c263..b0638a41bd0 100644
--- a/extensions/cli/src/messageConversion.test.ts
+++ b/extensions/cli/src/messageConversion.test.ts
@@ -1,5 +1,8 @@
 import type { ChatHistoryItem } from "core/index.js";
-import { convertFromUnifiedHistory } from "core/util/messageConversion.js";
+import {
+  convertFromUnifiedHistory,
+  convertFromUnifiedHistoryWithSystemMessage,
+} from "core/util/messageConversion.js";
 
 describe("convertFromUnifiedHistory", () => {
   it("should expand contextItems into user message content", () => {
@@ -139,3 +142,124 @@ describe("convertFromUnifiedHistory", () => {
     });
   });
 });
+
+describe("convertFromUnifiedHistoryWithSystemMessage", () => {
+  it("injects the system message at index 0", () => {
+    const historyItems: ChatHistoryItem[] = [
+      { message: { role: "user", content: "Hello" }, contextItems: [] },
+    ];
+
+    const result = convertFromUnifiedHistoryWithSystemMessage(
+      historyItems,
+      "You are a helpful assistant",
+    );
+
+    expect(result[0]).toEqual({
+      role: "system",
+      content: "You are a helpful assistant",
+    });
+    expect(result).toHaveLength(2);
+    expect(result[1].role).toBe("user");
+  });
+
+  it("does not leave a duplicate system message when history already starts with one", () => {
+    const historyItems: ChatHistoryItem[] = [
+      {
+        message: { role: "system", content: "Stored system" },
+        contextItems: [],
+      },
+      { message: { role: "user", content: "Hello" }, contextItems: [] },
+    ];
+
+    const result = convertFromUnifiedHistoryWithSystemMessage(
+      historyItems,
+      "Injected system",
+    );
+
+    const systemMessages = result.filter((m) => m.role === "system");
+    expect(systemMessages).toHaveLength(1);
+    expect(result[0]).toEqual({
+      role: "system",
+      content: "Injected system\n\nStored system",
+    });
+    // No system message should appear anywhere except index 0
+    result.slice(1).forEach((m) => expect(m.role).not.toBe("system"));
+  });
+
+  it("hoists a mid-conversation system message so it is not sent at a non-zero index (tool cancellation follow-up)", () => {
+    // Reproduces the "System message must be at the beginning" 400 error:
+    // a tool call is cancelled and a system notification lives mid-history.
+    const historyItems: ChatHistoryItem[] = [
+      {
+        message: { role: "user", content: "Run the command" },
+        contextItems: [],
+      },
+      {
+        message: {
+          role: "assistant",
+          content: "",
+          toolCalls: [
+            {
+              id: "tc-1",
+              type: "function",
+              function: { name: "run", arguments: "{}" },
+            },
+          ],
+        },
+        contextItems: [],
+        toolCallStates: [
+          {
+            toolCallId: "tc-1",
+            toolCall: {
+              id: "tc-1",
+              type: "function",
+              function: { name: "run", arguments: "{}" },
+            },
+            status: "canceled",
+            parsedArgs: {},
+          },
+        ],
+      },
+      {
+        message: {
+          role: "system",
+          content: "Chat history auto-compacted successfully.",
+        },
+        contextItems: [],
+      },
+    ];
+
+    const result = convertFromUnifiedHistoryWithSystemMessage(
+      historyItems,
+      "Base system",
+    );
+
+    // Only one system message, and it is first
+    expect(result[0].role).toBe("system");
+    result.slice(1).forEach((m) => expect(m.role).not.toBe("system"));
+    expect(result[0]).toEqual({
+      role: "system",
+      content: "Base system\n\nChat history auto-compacted successfully.",
+    });
+    // The cancelled tool call still produces a tool result message
+    expect(result.some((m) => m.role === "tool")).toBe(true);
+  });
+
+  it("emits a leading system message even when base system message is empty but history has one", () => {
+    const historyItems: ChatHistoryItem[] = [
+      {
+        message: { role: "system", content: "Only stored system" },
+        contextItems: [],
+      },
+      { message: { role: "user", content: "Hi" }, contextItems: [] },
+    ];
+
+    const result = convertFromUnifiedHistoryWithSystemMessage(historyItems, "");
+
+    expect(result[0]).toEqual({
+      role: "system",
+      content: "Only stored system",
+    });
+    expect(result.filter((m) => m.role === "system")).toHaveLength(1);
+  });
+});