diff --git a/source/common/http/http1/codec_impl.cc b/source/common/http/http1/codec_impl.cc
index ef6ece4380c2..ac1826a534b4 100644
--- a/source/common/http/http1/codec_impl.cc
+++ b/source/common/http/http1/codec_impl.cc
@@ -894,7 +894,7 @@ void ClientConnectionImpl::onMessageComplete() {
     // reused, unwind any outstanding readDisable() calls here. Only do this if there are no
     // pipelined responses remaining. Also do this before we dispatch end_stream in case the caller
     // immediately reuses the connection.
-    if (pending_responses_.empty()) {
+    if (connection_.state() == Network::Connection::State::Open && pending_responses_.empty()) {
       while (!connection_.readEnabled()) {
         connection_.readDisable(false);
       }
diff --git a/source/common/network/connection_impl.cc b/source/common/network/connection_impl.cc
index 15e76a9128e0..d7baebb26ef2 100644
--- a/source/common/network/connection_impl.cc
+++ b/source/common/network/connection_impl.cc
@@ -291,13 +291,12 @@ void ConnectionImpl::enableHalfClose(bool enabled) {
 }
 
 void ConnectionImpl::readDisable(bool disable) {
+  // Calls to readEnabled on a closed socket are considered to be an error.
   ASSERT(state() == State::Open);
-  if (state() != State::Open || file_event_ == nullptr) {
-    // If readDisable is called on a closed connection in error, do not crash.
-    return;
-  }
+  ASSERT(file_event_ != nullptr);
 
-  ENVOY_CONN_LOG(trace, "readDisable: enabled={} disable={}", *this, read_enabled_, disable);
+  ENVOY_CONN_LOG(trace, "readDisable: enabled={} disable={} state={}", *this, read_enabled_,
+                 disable, static_cast<int>(state()));
 
   // When we disable reads, we still allow for early close notifications (the equivalent of
   // EPOLLRDHUP for an epoll backend). For backends that support it, this allows us to apply
@@ -314,6 +313,11 @@ void ConnectionImpl::readDisable(bool disable) {
     ASSERT(read_enabled_);
     read_enabled_ = false;
 
+    if (state() != State::Open || file_event_ == nullptr) {
+      // If readDisable is called on a closed connection, do not crash.
+      return;
+    }
+
     // If half-close semantics are enabled, we never want early close notifications; we
     // always want to read all available data, even if the other side has closed.
     if (detect_early_close_ && !enable_half_close_) {
@@ -328,6 +332,12 @@ void ConnectionImpl::readDisable(bool disable) {
     }
     ASSERT(!read_enabled_);
     read_enabled_ = true;
+
+    if (state() != State::Open || file_event_ == nullptr) {
+      // If readDisable is called on a closed connection, do not crash.
+      return;
+    }
+
     // We never ask for both early close and read at the same time. If we are reading, we want to
     // consume all available data.
     file_event_->setEnabled(Event::FileReadyType::Read | Event::FileReadyType::Write);
@@ -358,7 +368,12 @@ void ConnectionImpl::raiseEvent(ConnectionEvent event) {
   }
 }
 
-bool ConnectionImpl::readEnabled() const { return read_enabled_; }
+bool ConnectionImpl::readEnabled() const {
+  // Calls to readEnabled on a closed socket are considered to be an error.
+  ASSERT(state() == State::Open);
+  ASSERT(file_event_ != nullptr);
+  return read_enabled_;
+}
 
 void ConnectionImpl::addConnectionCallbacks(ConnectionCallbacks& cb) { callbacks_.push_back(&cb); }
 
diff --git a/test/common/network/connection_impl_test.cc b/test/common/network/connection_impl_test.cc
index 272884e3f518..5f9a6dadcc47 100644
--- a/test/common/network/connection_impl_test.cc
+++ b/test/common/network/connection_impl_test.cc
@@ -570,15 +570,38 @@ TEST_P(ConnectionImplTest, KickUndone) {
   disconnect(true);
 }
 
-// Regression test for (at least one failure mode of)
-// https://github.com/envoyproxy/envoy/issues/3639 where readDisable on a close
-// connection caused a crash.
-TEST_P(ConnectionImplTest, ReadDisableAfterClose) {
+// Ensure that calls to readDisable on a closed connection are handled gracefully. Known past issues
+// include a crash on https://github.com/envoyproxy/envoy/issues/3639, and ASSERT failure followed
+// by infinite loop in https://github.com/envoyproxy/envoy/issues/9508
+TEST_P(ConnectionImplTest, ReadDisableAfterCloseHandledGracefully) {
   setUpBasicConnection();
-  disconnect(false);
 
+  client_connection_->readDisable(true);
+  client_connection_->readDisable(false);
+
+  client_connection_->readDisable(true);
+  client_connection_->readDisable(true);
+  client_connection_->readDisable(false);
+  client_connection_->readDisable(false);
+
+  client_connection_->readDisable(true);
+  client_connection_->readDisable(true);
+  disconnect(false);
+#ifndef NDEBUG
+  // When running in debug mode, verify that calls to readDisable and readEnabled on a closed socket
+  // trigger ASSERT failures.
+  EXPECT_DEBUG_DEATH(client_connection_->readEnabled(), "");
   EXPECT_DEBUG_DEATH(client_connection_->readDisable(true), "");
   EXPECT_DEBUG_DEATH(client_connection_->readDisable(false), "");
+#else
+  // When running in release mode, verify that calls to readDisable change the readEnabled state.
+  client_connection_->readDisable(false);
+  client_connection_->readDisable(true);
+  client_connection_->readDisable(false);
+  EXPECT_FALSE(client_connection_->readEnabled());
+  client_connection_->readDisable(false);
+  EXPECT_TRUE(client_connection_->readEnabled());
+#endif
 }
 
 TEST_P(ConnectionImplTest, EarlyCloseOnReadDisabledConnection) {
diff --git a/test/integration/integration_test.cc b/test/integration/integration_test.cc
index 91f38de55137..19f5b172edec 100644
--- a/test/integration/integration_test.cc
+++ b/test/integration/integration_test.cc
@@ -219,6 +219,31 @@ TEST_P(IntegrationTest, RouterUpstreamDisconnectBeforeResponseComplete) {
   testRouterUpstreamDisconnectBeforeResponseComplete();
 }
 
+// Regression test for https://github.com/envoyproxy/envoy/issues/9508
+TEST_P(IntegrationTest, ResponseFramedByConnectionCloseWithReadLimits) {
+  // Set a small buffer limit on the downstream in order to trigger a call to trigger readDisable on
+  // the upstream when proxying the response. Upstream limit needs to be larger so that
+  // RawBufferSocket::doRead reads the response body and detects the upstream close in the same call
+  // stack.
+  config_helper_.setBufferLimits(100000, 1);
+  initialize();
+
+  codec_client_ = makeHttpConnection(makeClientConnection((lookupPort("http"))));
+  fake_upstreams_[0]->set_allow_unexpected_disconnects(true);
+
+  auto response = codec_client_->makeHeaderOnlyRequest(default_request_headers_);
+  waitForNextUpstreamRequest();
+  // Disable chunk encoding to trigger framing by connection close.
+  upstream_request_->encodeHeaders(Http::TestHeaderMapImpl{{":status", "200"}, {":no-chunks", "1"}},
+                                   false);
+  upstream_request_->encodeData(512, true);
+  ASSERT_TRUE(fake_upstream_connection_->close());
+
+  response->waitForEndStream();
+
+  EXPECT_TRUE(response->complete());
+}
+
 TEST_P(IntegrationTest, RouterDownstreamDisconnectBeforeRequestComplete) {
   testRouterDownstreamDisconnectBeforeRequestComplete();
 }