diff --git a/include/envoy/server/api_listener.h b/include/envoy/server/api_listener.h
index da5937f5d680a..d07dd2ec8fd2c 100644
--- a/include/envoy/server/api_listener.h
+++ b/include/envoy/server/api_listener.h
@@ -21,6 +21,13 @@ class ApiListener {
    */
   virtual absl::string_view name() const PURE;
 
+  /**
+   * Shutdown the ApiListener. This is an interrupt, not a drain. In other words, calling this
+   * function results in termination of all active streams vs. draining where no new streams are
+   * allowed, but already existing streams are allowed to finish.
+   */
+  virtual void shutdown() PURE;
+
   /**
    * @return the Type of the ApiListener.
    */
diff --git a/source/server/api_listener_impl.cc b/source/server/api_listener_impl.cc
index f990254683815..107afabcadb2c 100644
--- a/source/server/api_listener_impl.cc
+++ b/source/server/api_listener_impl.cc
@@ -25,6 +25,13 @@ ApiListenerImplBase::ApiListenerImplBase(const envoy::config::listener::v3::List
       factory_context_(parent_.server_, config_, *this, *global_scope_, *listener_scope_),
       read_callbacks_(SyntheticReadCallbacks(*this)) {}
 
+void ApiListenerImplBase::SyntheticReadCallbacks::SyntheticConnection::raiseConnectionEvent(
+    Network::ConnectionEvent event) {
+  for (Network::ConnectionCallbacks* callback : callbacks_) {
+    callback->onEvent(event);
+  }
+}
+
 HttpApiListener::HttpApiListener(const envoy::config::listener::v3::Listener& config,
                                  ListenerManagerImpl& parent, const std::string& name)
     : ApiListenerImplBase(config, parent, name) {
@@ -44,5 +51,12 @@ Http::ApiListenerOptRef HttpApiListener::http() {
   return Http::ApiListenerOptRef(std::ref(*http_connection_manager_));
 }
 
+void HttpApiListener::shutdown() {
+  // The Http::ConnectionManagerImpl is a callback target for the read_callback_.connection_. By
+  // raising connection closure, Http::ConnectionManagerImpl::onEvent is fired. In that case the
+  // Http::ConnectionManagerImpl will reset any ActiveStreams it has.
+  read_callbacks_.connection_.raiseConnectionEvent(Network::ConnectionEvent::RemoteClose);
+}
+
 } // namespace Server
 } // namespace Envoy
diff --git a/source/server/api_listener_impl.h b/source/server/api_listener_impl.h
index 3b5dfdcded010..9227f21810860 100644
--- a/source/server/api_listener_impl.h
+++ b/source/server/api_listener_impl.h
@@ -75,6 +75,8 @@ class ApiListenerImplBase : public ApiListener,
           : parent_(parent), stream_info_(parent_.parent_.factory_context_.timeSource()),
             options_(std::make_shared<std::vector<Network::Socket::OptionConstSharedPtr>>()) {}
 
+      void raiseConnectionEvent(Network::ConnectionEvent event);
+
       // Network::FilterManager
       void addWriteFilter(Network::WriteFilterSharedPtr) override {
         NOT_IMPLEMENTED_GCOVR_EXCL_LINE;
@@ -84,7 +86,9 @@ class ApiListenerImplBase : public ApiListener,
       bool initializeReadFilters() override { return true; }
 
       // Network::Connection
-      void addConnectionCallbacks(Network::ConnectionCallbacks&) override {}
+      void addConnectionCallbacks(Network::ConnectionCallbacks& cb) override {
+        callbacks_.push_back(&cb);
+      }
       void addBytesSentCallback(Network::Connection::BytesSentCb) override {
         NOT_IMPLEMENTED_GCOVR_EXCL_LINE;
       }
@@ -129,6 +133,7 @@ class ApiListenerImplBase : public ApiListener,
       SyntheticReadCallbacks& parent_;
       StreamInfo::StreamInfoImpl stream_info_;
       Network::ConnectionSocket::OptionsSharedPtr options_;
+      std::list<Network::ConnectionCallbacks*> callbacks_;
     };
 
     ApiListenerImplBase& parent_;
@@ -157,6 +162,9 @@ class HttpApiListener : public ApiListenerImplBase {
   // ApiListener
   ApiListener::Type type() const override { return ApiListener::Type::HttpApiListener; }
   Http::ApiListenerOptRef http() override;
+  void shutdown() override;
+
+  Network::ReadFilterCallbacks& readCallbacksForTest() { return read_callbacks_; }
 
 private:
   // Need to store the factory due to the shared_ptrs that need to be kept alive: date provider,
diff --git a/source/server/server.cc b/source/server/server.cc
index 32d38f7916f6f..024e7c5d23710 100644
--- a/source/server/server.cc
+++ b/source/server/server.cc
@@ -578,6 +578,13 @@ void InstanceImpl::terminate() {
 
   // Shutdown all the workers now that the main dispatch loop is done.
   if (listener_manager_ != nullptr) {
+    // Also shutdown the listener manager's ApiListener, if there is one, which runs on the main
+    // thread. This needs to happen ahead of calling thread_local_.shutdown() below to prevent any
+    // objects in the ApiListener destructor to reference any objects in thread local storage.
+    if (listener_manager_->apiListener().has_value()) {
+      listener_manager_->apiListener()->get().shutdown();
+    }
+
     listener_manager_->stopWorkers();
   }
 
diff --git a/test/integration/api_listener_integration_test.cc b/test/integration/api_listener_integration_test.cc
index ee1e2d672dab1..1a9e04ef072b0 100644
--- a/test/integration/api_listener_integration_test.cc
+++ b/test/integration/api_listener_integration_test.cc
@@ -30,7 +30,6 @@ class ApiListenerIntegrationTest : public BaseIntegrationTest,
       bootstrap.mutable_static_resources()->add_listeners()->MergeFrom(
           Server::parseListenerFromV2Yaml(api_listener_config()));
     });
-    BaseIntegrationTest::initialize();
   }
 
   void TearDown() override {
@@ -84,6 +83,7 @@ INSTANTIATE_TEST_SUITE_P(IpVersions, ApiListenerIntegrationTest,
                          TestUtility::ipTestParamsToString);
 
 TEST_P(ApiListenerIntegrationTest, Basic) {
+  BaseIntegrationTest::initialize();
   absl::Notification done;
   test_server_->server().dispatcher().post([this, &done]() -> void {
     ASSERT_TRUE(test_server_->server().listenerManager().apiListener().has_value());
@@ -111,5 +111,33 @@ TEST_P(ApiListenerIntegrationTest, Basic) {
   ASSERT_TRUE(done.WaitForNotificationWithTimeout(absl::Seconds(1)));
 }
 
+TEST_P(ApiListenerIntegrationTest, DestroyWithActiveStreams) {
+  autonomous_allow_incomplete_streams_ = true;
+  BaseIntegrationTest::initialize();
+  absl::Notification done;
+
+  test_server_->server().dispatcher().post([this, &done]() -> void {
+    ASSERT_TRUE(test_server_->server().listenerManager().apiListener().has_value());
+    ASSERT_EQ("api_listener", test_server_->server().listenerManager().apiListener()->get().name());
+    ASSERT_TRUE(test_server_->server().listenerManager().apiListener()->get().http().has_value());
+    auto& http_api_listener =
+        test_server_->server().listenerManager().apiListener()->get().http()->get();
+
+    ON_CALL(stream_encoder_, getStream()).WillByDefault(ReturnRef(stream_encoder_.stream_));
+    auto& stream_decoder = http_api_listener.newStream(stream_encoder_);
+
+    // Send a headers-only request
+    stream_decoder.decodeHeaders(
+        Http::HeaderMapPtr(new Http::TestHeaderMapImpl{
+            {":method", "GET"}, {":path", "/api"}, {":scheme", "http"}, {":authority", "host"}}),
+        false);
+
+    done.Notify();
+  });
+  ASSERT_TRUE(done.WaitForNotificationWithTimeout(absl::Seconds(1)));
+  // The server should shutdown the ApiListener at the right time during server termination such
+  // that no crashes occur if termination happens when the ApiListener still has ongoing streams.
+}
+
 } // namespace
-} // namespace Envoy
\ No newline at end of file
+} // namespace Envoy
diff --git a/test/server/BUILD b/test/server/BUILD
index 400c4b80fab88..358ec824569c0 100644
--- a/test/server/BUILD
+++ b/test/server/BUILD
@@ -23,6 +23,7 @@ envoy_cc_test(
         ":utility_lib",
         "//source/server:api_listener_lib",
         "//source/server:listener_lib",
+        "//test/mocks/network:network_mocks",
         "//test/mocks/server:server_mocks",
         "//test/test_common:utility_lib",
         "@envoy_api//envoy/config/listener/v3:pkg_cc_proto",
diff --git a/test/server/api_listener_test.cc b/test/server/api_listener_test.cc
index ccf9c643ee551..f229823c59c32 100644
--- a/test/server/api_listener_test.cc
+++ b/test/server/api_listener_test.cc
@@ -5,6 +5,7 @@
 #include "server/api_listener_impl.h"
 #include "server/listener_manager_impl.h"
 
+#include "test/mocks/network/mocks.h"
 #include "test/mocks/server/mocks.h"
 #include "test/server/utility.h"
 #include "test/test_common/utility.h"
@@ -87,5 +88,48 @@ name: test_api_listener
       "eds_cluster_config {\n    eds_config {\n      path: \"eds path\"\n    }\n  }\n}\n");
 }
 
+TEST_F(ApiListenerTest, HttpApiListenerShutdown) {
+  const std::string yaml = R"EOF(
+name: test_api_listener
+address:
+  socket_address:
+    address: 127.0.0.1
+    port_value: 1234
+api_listener:
+  api_listener:
+    "@type": type.googleapis.com/envoy.config.filter.network.http_connection_manager.v2.HttpConnectionManager
+    stat_prefix: hcm
+    route_config:
+      name: api_router
+      virtual_hosts:
+        - name: api
+          domains:
+            - "*"
+          routes:
+            - match:
+                prefix: "/"
+              route:
+                cluster: dynamic_forward_proxy_cluster
+  )EOF";
+
+  const envoy::config::listener::v3::Listener config = parseListenerFromV2Yaml(yaml);
+
+  auto http_api_listener = HttpApiListener(config, *listener_manager_, config.name());
+
+  ASSERT_EQ("test_api_listener", http_api_listener.name());
+  ASSERT_EQ(ApiListener::Type::HttpApiListener, http_api_listener.type());
+  ASSERT_TRUE(http_api_listener.http().has_value());
+
+  Network::MockConnectionCallbacks network_connection_callbacks;
+  // TODO(junr03): potentially figure out a way of unit testing this behavior without exposing a
+  // ForTest function.
+  http_api_listener.readCallbacksForTest().connection().addConnectionCallbacks(
+      network_connection_callbacks);
+
+  EXPECT_CALL(network_connection_callbacks, onEvent(Network::ConnectionEvent::RemoteClose));
+  // Shutting down the ApiListener should raise an event on all connection callback targets.
+  http_api_listener.shutdown();
+}
+
 } // namespace Server
-} // namespace Envoy
\ No newline at end of file
+} // namespace Envoy