diff --git a/lambdas/functions/control-plane/src/scale-runners/scale-down.test.ts b/lambdas/functions/control-plane/src/scale-runners/scale-down.test.ts
index 2dfb190a38..0d0d0ac708 100644
--- a/lambdas/functions/control-plane/src/scale-runners/scale-down.test.ts
+++ b/lambdas/functions/control-plane/src/scale-runners/scale-down.test.ts
@@ -336,6 +336,82 @@ describe('Scale down runners', () => {
         checkNonTerminated(runners);
       });
 
+      it(`Should not terminate a runner that became busy between deregister and post-deregister check.`, async () => {
+        // setup: runner appears idle on first check, deregister succeeds,
+        // but post-deregister re-check finds it busy (race condition)
+        const runners = [
+          createRunnerTestData(
+            'race-condition-1',
+            type,
+            MINIMUM_TIME_RUNNING_IN_MINUTES + 1,
+            true,
+            false,
+            false,
+          ),
+        ];
+
+        mockGitHubRunners(runners);
+        mockAwsRunners(runners);
+
+        // First call returns not-busy (pre-deregister), second returns busy (post-deregister)
+        let callCount = 0;
+        const busyCheckMock = () => {
+          callCount++;
+          if (callCount <= 1) {
+            return { data: { busy: false } };
+          }
+          return { data: { busy: true } };
+        };
+        mockOctokit.actions.getSelfHostedRunnerForRepo.mockImplementation(busyCheckMock);
+        mockOctokit.actions.getSelfHostedRunnerForOrg.mockImplementation(busyCheckMock);
+
+        // act
+        await expect(scaleDown()).resolves.not.toThrow();
+
+        // assert: runner should NOT be terminated
+        checkTerminated(runners);
+        checkNonTerminated(runners);
+      });
+
+      it(`Should terminate a runner when post-deregister busy check returns 404.`, async () => {
+        // setup: after deregistration, GitHub API returns 404 (runner fully removed)
+        const runners = [
+          createRunnerTestData(
+            'deregistered-404',
+            type,
+            MINIMUM_TIME_RUNNING_IN_MINUTES + 1,
+            true,
+            false,
+            true,
+          ),
+        ];
+
+        mockGitHubRunners(runners);
+        mockAwsRunners(runners);
+
+        // First call returns not-busy, second throws 404
+        let callCount = 0;
+        const busyCheckMock = () => {
+          callCount++;
+          if (callCount <= 1) {
+            return { data: { busy: false } };
+          }
+          const error = new Error('Not Found');
+          (error as any).status = 404;
+          Object.setPrototypeOf(error, RequestError.prototype);
+          throw error;
+        };
+        mockOctokit.actions.getSelfHostedRunnerForRepo.mockImplementation(busyCheckMock);
+        mockOctokit.actions.getSelfHostedRunnerForOrg.mockImplementation(busyCheckMock);
+
+        // act
+        await expect(scaleDown()).resolves.not.toThrow();
+
+        // assert: runner should be terminated (404 = not busy)
+        checkTerminated(runners);
+        checkNonTerminated(runners);
+      });
+
       it(`Should terminate orphan (Non JIT)`, async () => {
         // setup
         const orphanRunner = createRunnerTestData('orphan-1', type, MINIMUM_BOOT_TIME + 1, false, false, false);
diff --git a/lambdas/functions/control-plane/src/scale-runners/scale-down.ts b/lambdas/functions/control-plane/src/scale-runners/scale-down.ts
index 6086af7714..85e5ea8b4e 100644
--- a/lambdas/functions/control-plane/src/scale-runners/scale-down.ts
+++ b/lambdas/functions/control-plane/src/scale-runners/scale-down.ts
@@ -138,39 +138,63 @@ async function removeRunner(ec2runner: RunnerInfo, ghRunnerIds: number[]): Promi
       return;
     }
 
+    // Step 1: Check busy state as a fast-path to skip runners that are obviously busy.
     const states = await Promise.all(
       ghRunnerIds.map(async (ghRunnerId) => {
-        // Get busy state instead of using the output of listGitHubRunners(...) to minimize to race condition.
         return await getGitHubRunnerBusyState(githubAppClient, ec2runner, ghRunnerId);
       }),
     );
 
-    if (states.every((busy) => busy === false)) {
-      const statuses = await Promise.all(
-        ghRunnerIds.map(async (ghRunnerId) => {
-          return (
-            ec2runner.type === 'Org'
-              ? await githubAppClient.actions.deleteSelfHostedRunnerFromOrg({
-                  runner_id: ghRunnerId,
-                  org: ec2runner.owner,
-                })
-              : await githubAppClient.actions.deleteSelfHostedRunnerFromRepo({
-                  runner_id: ghRunnerId,
-                  owner: ec2runner.owner.split('/')[0],
-                  repo: ec2runner.owner.split('/')[1],
-                })
-          ).status;
-        }),
-      );
+    if (!states.every((busy) => busy === false)) {
+      logger.info(`Runner '${ec2runner.instanceId}' cannot be de-registered, because it is still busy.`);
+      return;
+    }
 
-      if (statuses.every((status) => status == 204)) {
-        await terminateRunner(ec2runner.instanceId);
-        logger.info(`AWS runner instance '${ec2runner.instanceId}' is terminated and GitHub runner is de-registered.`);
-      } else {
-        logger.error(`Failed to de-register GitHub runner: ${statuses}`);
-      }
+    // Step 2: De-register the runner from GitHub. This prevents GitHub from assigning new jobs
+    // to this runner, closing the race window where a job could be assigned between the busy
+    // check above and the termination below.
+    const statuses = await Promise.all(
+      ghRunnerIds.map(async (ghRunnerId) => {
+        return (
+          ec2runner.type === 'Org'
+            ? await githubAppClient.actions.deleteSelfHostedRunnerFromOrg({
+                runner_id: ghRunnerId,
+                org: ec2runner.owner,
+              })
+            : await githubAppClient.actions.deleteSelfHostedRunnerFromRepo({
+                runner_id: ghRunnerId,
+                owner: ec2runner.owner.split('/')[0],
+                repo: ec2runner.owner.split('/')[1],
+              })
+        ).status;
+      }),
+    );
+
+    if (!statuses.every((status) => status == 204)) {
+      logger.error(`Failed to de-register GitHub runner: ${statuses}`);
+      return;
+    }
+
+    // Step 3: Re-check busy state after de-registration. A job may have been assigned between
+    // step 1 and step 2. After de-registration no new jobs can be assigned, so this check is
+    // now stable. If the runner is busy, the in-flight job will complete using its job-scoped
+    // OAuth token (the runner worker uses credentials from the job message, not the runner
+    // registration). We leave the instance running and it will be cleaned up as an orphan.
+    const postDeregisterStates = await Promise.all(
+      ghRunnerIds.map(async (ghRunnerId) => {
+        return await getGitHubRunnerBusyState(githubAppClient, ec2runner, ghRunnerId);
+      }),
+    );
+
+    if (postDeregisterStates.every((busy) => busy === false)) {
+      await terminateRunner(ec2runner.instanceId);
+      logger.info(`AWS runner instance '${ec2runner.instanceId}' is terminated and GitHub runner is de-registered.`);
     } else {
-      logger.info(`Runner '${ec2runner.instanceId}' cannot be de-registered, because it is still busy.`);
+      logger.warn(
+        `Runner '${ec2runner.instanceId}' became busy between idle check and de-registration. ` +
+          `Skipping termination to allow the in-flight job to complete. ` +
+          `The instance will be cleaned up as an orphan on a subsequent cycle.`,
+      );
     }
   } catch (e) {
     logger.error(`Runner '${ec2runner.instanceId}' cannot be de-registered. Error: ${e}`, {