diff --git a/.changeset/large-ladybugs-breathe.md b/.changeset/large-ladybugs-breathe.md
new file mode 100644
index 00000000000..7eb1d1d965a
--- /dev/null
+++ b/.changeset/large-ladybugs-breathe.md
@@ -0,0 +1,5 @@
+---
+"@apollo/server": patch
+---
+
+Catch errors thrown by subscription generators, and gracefully clean up the subscription instead of crashing.
diff --git a/packages/server/src/__tests__/plugin/subscriptionCallback/index.test.ts b/packages/server/src/__tests__/plugin/subscriptionCallback/index.test.ts
index 65d380c2c11..ea12d27eeff 100644
--- a/packages/server/src/__tests__/plugin/subscriptionCallback/index.test.ts
+++ b/packages/server/src/__tests__/plugin/subscriptionCallback/index.test.ts
@@ -1102,6 +1102,62 @@ describe('SubscriptionCallbackPlugin', () => {
     `);
   });
 
+  it('sends a `complete` with errors when a subscription throws an error', async () => {
+    const server = await startSubscriptionServer({ logger });
+
+    mockRouterCheckResponse();
+    mockRouterCheckResponse();
+    mockRouterCompleteResponse({
+      errors: [{ message: "The subscription generator didn't catch this!" }],
+    });
+
+    const result = await server.executeHTTPGraphQLRequest(
+      buildHTTPGraphQLRequest({
+        body: {
+          query: `#graphql
+            subscription {
+              throwsError
+            }
+          `,
+          extensions: {
+            subscription: {
+              callbackUrl: 'http://mock-router-url.com',
+              subscriptionId: '1234-cats',
+              verifier: 'my-verifier-token',
+            },
+          },
+        },
+      }),
+    );
+    expect(result.status).toEqual(200);
+
+    jest.advanceTimersByTime(5000);
+    await server.stop();
+
+    expect(logger.orderOfOperations).toMatchInlineSnapshot(`
+      [
+        "SubscriptionCallback[1234-cats]: Received new subscription request",
+        "SubscriptionManager[1234-cats]: Sending \`check\` request to router",
+        "SubscriptionManager[1234-cats]: \`check\` request successful",
+        "SubscriptionCallback[1234-cats]: Starting graphql-js subscription",
+        "SubscriptionCallback[1234-cats]: graphql-js subscription successful",
+        "SubscriptionManager[1234-cats]: Starting new heartbeat interval for http://mock-router-url.com",
+        "SubscriptionManager[1234-cats]: Listening to graphql-js subscription",
+        "SubscriptionCallback[1234-cats]: Responding to original subscription request",
+        "ERROR: SubscriptionManager[1234-cats]: Generator threw an error, terminating subscription: The subscription generator didn't catch this!",
+        "SubscriptionManager[1234-cats]: Sending \`complete\` request to router with errors",
+        "SubscriptionManager: Sending \`check\` request to http://mock-router-url.com for ID: 1234-cats",
+        "SubscriptionCallback: Server is shutting down. Cleaning up outstanding subscriptions and heartbeat intervals",
+        "SubscriptionManager[1234-cats]: \`complete\` request successful",
+        "SubscriptionManager: Terminating subscriptions for ID: 1234-cats",
+        "SubscriptionManager: Terminating heartbeat interval for http://mock-router-url.com",
+        "SubscriptionManager: Heartbeat received response for ID: 1234-cats",
+        "SubscriptionManager: Heartbeat request successful, ID: 1234-cats",
+        "SubscriptionCallback: Successfully cleaned up outstanding subscriptions and heartbeat intervals.",
+      ]
+    `);
+  });
+
   (process.env.INCREMENTAL_DELIVERY_TESTS_ENABLED ? describe.skip : describe)(
     'error handling',
     () => {
@@ -1979,6 +2035,7 @@ async function startSubscriptionServer(
       type Subscription {
         count: Int
         terminatesSuccessfully: Boolean
+        throwsError: Int
       }
     `,
     resolvers: {
@@ -2011,6 +2068,19 @@ async function startSubscriptionServer(
             },
           }),
         },
+        throwsError: {
+          subscribe: () => ({
+            [Symbol.asyncIterator]() {
+              return {
+                next: () => {
+                  throw new Error(
+                    "The subscription generator didn't catch this!",
+                  );
+                },
+              };
+            },
+          }),
+        },
       },
     },
     ...opts,
diff --git a/packages/server/src/plugin/subscriptionCallback/index.ts b/packages/server/src/plugin/subscriptionCallback/index.ts
index 33258d751e0..159f9cb7c75 100644
--- a/packages/server/src/plugin/subscriptionCallback/index.ts
+++ b/packages/server/src/plugin/subscriptionCallback/index.ts
@@ -557,39 +557,48 @@ class SubscriptionManager {
       cancelled: false,
       async startConsumingSubscription() {
         self.logger?.debug(`Listening to graphql-js subscription`, id);
-        for await (const payload of subscription) {
-          if (this.cancelled) {
-            self.logger?.debug(
-              `Subscription already cancelled, ignoring current and future payloads`,
-              id,
-            );
-            // It's already been cancelled - something else has already handled
-            // sending the `complete` request so we don't want to `break` here
-            // and send it again after the loop.
-            return;
-          }
+        try {
+          for await (const payload of subscription) {
+            if (this.cancelled) {
+              self.logger?.debug(
+                `Subscription already cancelled, ignoring current and future payloads`,
+                id,
+              );
+              // It's already been cancelled - something else has already handled
+              // sending the `complete` request so we don't want to `break` here
+              // and send it again after the loop.
+              return;
+            }
 
-          try {
-            await self.retryFetch({
-              url: callbackUrl,
-              action: 'next',
-              id,
-              verifier,
-              payload,
-            });
-          } catch (e) {
-            const originalError = ensureError(e);
-            self.logger?.error(
-              `\`next\` request failed, terminating subscription: ${originalError.message}`,
-              id,
-            );
-            self.terminateSubscription(id, callbackUrl);
+            try {
+              await self.retryFetch({
+                url: callbackUrl,
+                action: 'next',
+                id,
+                verifier,
+                payload,
+              });
+            } catch (e) {
+              const originalError = ensureError(e);
+              self.logger?.error(
+                `\`next\` request failed, terminating subscription: ${originalError.message}`,
+                id,
+              );
+              self.terminateSubscription(id, callbackUrl);
+            }
           }
+          // The subscription ended without errors, send the `complete` request to
+          // the router
+          self.logger?.debug(`Subscription completed without errors`, id);
+          await this.completeSubscription();
+        } catch (e) {
+          const error = ensureGraphQLError(e);
+          self.logger?.error(
+            `Generator threw an error, terminating subscription: ${error.message}`,
+            id,
+          );
+          this.completeSubscription([error]);
         }
-        // The subscription ended without errors, send the `complete` request to
-        // the router
-        self.logger?.debug(`Subscription completed without errors`, id);
-        await this.completeSubscription();
       },
       async completeSubscription(errors?: readonly GraphQLError[]) {
         if (this.cancelled) return;