diff --git a/packages/agent/src/adapters/error-classification.ts b/packages/agent/src/adapters/error-classification.ts
index 4873724de0..5adf8d40e2 100644
--- a/packages/agent/src/adapters/error-classification.ts
+++ b/packages/agent/src/adapters/error-classification.ts
@@ -1,3 +1,5 @@
+import { getErrorMessage } from "@posthog/shared";
+
 export type AgentErrorClassification =
   | "upstream_stream_terminated"
   | "upstream_connection_error"
@@ -32,3 +34,8 @@ export function classifyAgentError(
   }
   return "agent_error";
 }
+
+/** Hard API rejection: the assembled prompt exceeds the model's context window. */
+export function isPromptTooLongError(error: unknown): boolean {
+  return /prompt is too long/i.test(getErrorMessage(error));
+}
diff --git a/packages/agent/src/server/agent-server.test.ts b/packages/agent/src/server/agent-server.test.ts
index 961deee65b..8766bcd3bf 100644
--- a/packages/agent/src/server/agent-server.test.ts
+++ b/packages/agent/src/server/agent-server.test.ts
@@ -1808,6 +1808,98 @@ describe("AgentServer HTTP Mode", () => {
   });
 
   describe("native resume", () => {
+    it.each([
+      { retryOutcome: "succeeds", retryFails: false },
+      { retryOutcome: "fails", retryFails: true },
+    ])(
+      "clears resume state when the fresh-session retry $retryOutcome",
+      async ({ retryFails }) => {
+        const s = createServer();
+        await s.start();
+
+        const prompts: ContentBlock[][] = [];
+        const prompt = vi.fn(async (params: { prompt: ContentBlock[] }) => {
+          prompts.push(params.prompt);
+          if (prompts.length === 1) {
+            throw new Error("Internal error: Prompt is too long");
+          }
+          if (retryFails) {
+            throw new Error("Fresh-session retry failed");
+          }
+          return { stopReason: "end_turn" };
+        });
+        const newSession = vi.fn(async () => ({ sessionId: "fresh-session" }));
+
+        const internals = s as unknown as {
+          session: {
+            acpSessionId: string;
+            clientConnection: {
+              prompt: typeof prompt;
+              newSession: typeof newSession;
+            };
+          };
+          resumeState: ResumeState | null;
+          nativeResume: { sessionId: string; warm: boolean } | null;
+          loadResumeState(
+            taskId: string,
+            resumeRunId: string,
+            runId: string,
+          ): Promise<void>;
+          sendResumeContinuation(
+            payload: JwtPayload,
+            taskRun: TaskRun | null,
+          ): Promise<void>;
+        };
+        internals.session.clientConnection.prompt = prompt;
+        internals.session.clientConnection.newSession = newSession;
+        internals.nativeResume = { sessionId: "prior-session", warm: true };
+        internals.loadResumeState = vi.fn(async () => {
+          internals.resumeState = {
+            conversation: [
+              {
+                role: "user",
+                content: [{ type: "text", text: "original task" }],
+              },
+              {
+                role: "assistant",
+                content: [{ type: "text", text: "progress so far" }],
+              },
+            ],
+            latestGitCheckpoint: null,
+            interrupted: false,
+            logEntryCount: 2,
+            sessionId: "prior-session",
+          };
+        });
+
+        await internals.sendResumeContinuation(
+          {
+            task_id: "test-task-id",
+            run_id: "test-run-id",
+            team_id: 1,
+            user_id: 1,
+            distinct_id: "test-distinct-id",
+            mode: "interactive",
+          },
+          createTaskRun({
+            id: "test-run-id",
+            state: { resume_from_run_id: "previous-run" },
+          }),
+        );
+
+        expect(newSession).toHaveBeenCalledOnce();
+        expect(internals.session.acpSessionId).toBe("fresh-session");
+        expect(internals.resumeState).toBeNull();
+        expect(internals.nativeResume).toBeNull();
+        expect(prompts).toHaveLength(2);
+        const retryText = prompts[1]
+          .map((block) => ("text" in block ? block.text : ""))
+          .join("\n");
+        expect(retryText).toContain("progress so far");
+      },
+      20000,
+    );
+
     it("hydrates cold sessions from S3 logs instead of cached resume conversation", async () => {
       const originalConfigDir = process.env.CLAUDE_CONFIG_DIR;
       process.env.CLAUDE_CONFIG_DIR = join(repo.path, ".claude-test");
diff --git a/packages/agent/src/server/agent-server.ts b/packages/agent/src/server/agent-server.ts
index 75fa3d1ba3..912414ada6 100644
--- a/packages/agent/src/server/agent-server.ts
+++ b/packages/agent/src/server/agent-server.ts
@@ -19,6 +19,7 @@ import { getCurrentBranch } from "@posthog/git/queries";
 import {
   type Adapter,
   buildPrOutput,
+  getErrorMessage,
   mergePrUrls,
   readPrUrls,
 } from "@posthog/shared";
@@ -40,6 +41,7 @@ import { hasCodexThreadState } from "../adapters/codex-app-server/thread-state";
 import {
   type AgentErrorClassification,
   classifyAgentError,
+  isPromptTooLongError,
 } from "../adapters/error-classification";
 import {
   SIGNED_COMMIT_QUALIFIED_TOOL_NAME,
@@ -249,6 +251,8 @@ interface ActiveSession {
   /** Whether a desktop client has ever connected via SSE during this session */
   hasDesktopConnected: boolean;
   pendingHandoffGitState?: HandoffLocalGitState;
+  /** Meta the session was created with, reused when a retry needs a fresh session */
+  sessionMeta: Record<string, unknown>;
 }
 
 interface InstalledSkillBundle {
@@ -328,6 +332,7 @@ export class AgentServer {
   private lastReportedBranch: string | null = null;
   private resumeState: ResumeState | null = null;
   private nativeResume: { sessionId: string; warm: boolean } | null = null;
+  private oversizedResumeRetried = false;
   // Prewarmed runs boot before the user's first message exists, so the boot-time
   // --autoPublish flag can't carry the user's choice; it is resolved from run
   // state when the first message arrives (see resolveWarmAutoPublishUpgrade).
@@ -1409,6 +1414,7 @@ export class AgentServer {
       permissionMode: initialPermissionMode,
       hasDesktopConnected: sseController !== null,
       pendingHandoffGitState: undefined,
+      sessionMeta,
     };
 
     this.logger = new Logger({
@@ -1745,7 +1751,6 @@ export class AgentServer {
         gitCheckpointBranch: resumeState.latestGitCheckpoint?.branch ?? null,
       });
 
-      this.resumeState = null;
       return {
         prompt: resumePromptBlocks,
         ...(resumePromptMeta ? { meta: resumePromptMeta } : {}),
@@ -1786,21 +1791,82 @@ export class AgentServer {
           hasPendingUserMessage: !!pendingUserPrompt?.prompt.length,
         });
 
-        this.resumeState = null;
-        this.nativeResume = null;
         return {
           prompt,
           ...(pendingUserPrompt?.meta ? { meta: pendingUserPrompt.meta } : {}),
         };
       },
+      { retryOnOversizedPrompt: true },
     );
   }
 
+  /**
+   * A native resume replays the prior transcript verbatim; when that
+   * transcript no longer fits the context window, every request (including
+   * auto-compaction) is rejected, so the only way forward is a fresh session
+   * seeded with the summarized history the non-native resume path uses.
+   */
+  private async retryOversizedResumeOnFreshSession(
+    payload: JwtPayload,
+    taskRun: TaskRun | null,
+  ): Promise<boolean> {
+    if (this.oversizedResumeRetried || !this.session) {
+      return false;
+    }
+    this.oversizedResumeRetried = true;
+
+    const resumeRunId = this.getResumeRunId(taskRun);
+    if (!resumeRunId) return false;
+    if (!this.resumeState) {
+      try {
+        await this.loadResumeState(
+          payload.task_id,
+          resumeRunId,
+          payload.run_id,
+        );
+      } catch (error) {
+        this.logger.warn("Failed to reload resume state for retry", {
+          error: getErrorMessage(error),
+        });
+        return false;
+      }
+    }
+    if (!this.resumeState?.conversation.length) return false;
+
+    this.logger.warn(
+      "Resume prompt exceeded the context window; retrying on a fresh session with summarized history",
+      { taskId: payload.task_id, runId: payload.run_id },
+    );
+
+    try {
+      const response = await this.session.clientConnection.newSession({
+        cwd: this.config.repositoryPath ?? "/tmp/workspace",
+        mcpServers: this.config.mcpServers ?? [],
+        _meta: this.session.sessionMeta,
+      });
+      this.session.acpSessionId = response.sessionId;
+    } catch (error) {
+      this.logger.warn("Failed to start fresh session for oversized resume", {
+        error: getErrorMessage(error),
+      });
+      return false;
+    }
+
+    try {
+      await this.sendResumeMessage(payload, taskRun);
+      return true;
+    } finally {
+      this.resumeState = null;
+      this.nativeResume = null;
+    }
+  }
+
   private async runResumeTurn(
     payload: JwtPayload,
     taskRun: TaskRun | null,
     logLabel: string,
     buildPrompt: () => Promise<BuiltPrompt>,
+    opts: { retryOnOversizedPrompt?: boolean } = {},
   ): Promise<void> {
     if (!this.session) return;
 
@@ -1819,6 +1885,10 @@ export class AgentServer {
         stopReason: result.stopReason,
       });
 
+      // Kept until the turn succeeds so a prompt-too-long retry can reuse it.
+      this.resumeState = null;
+      this.nativeResume = null;
+
       await this.clearPendingInitialPromptState(payload, taskRun);
 
       if (result.stopReason === "end_turn") {
@@ -1836,6 +1906,13 @@ export class AgentServer {
       if (this.session) {
         await this.session.logWriter.flushAll();
       }
+      if (
+        opts.retryOnOversizedPrompt &&
+        isPromptTooLongError(error) &&
+        (await this.retryOversizedResumeOnFreshSession(payload, taskRun))
+      ) {
+        return;
+      }
       await this.handleTurnFailure(payload, "resume", error);
     }
   }