diff --git a/lldb/include/lldb/Host/JSONTransport.h b/lldb/include/lldb/Host/JSONTransport.h
index 6b114ee497a8b..c3a90cb0c3364 100644
--- a/lldb/include/lldb/Host/JSONTransport.h
+++ b/lldb/include/lldb/Host/JSONTransport.h
@@ -259,9 +259,11 @@ template <typename Proto> class IOTransport : public JSONTransport<Proto> {
       if (!m_buffer.empty())
         handler.OnError(llvm::make_error<TransportUnhandledContentsError>(
             std::string(m_buffer.str())));
+      // Move the read handle to a local before notifying the handler. The
+      // handler may destroy this transport (e.g. by erasing it from a
+      // connection map), so accessing members after OnClosed() is unsafe.
+      auto read_handle = std::move(m_read_handle);
       handler.OnClosed();
-      // On EOF, remove the read handle from the MainLoop.
-      m_read_handle.reset();
     }
   }
 
diff --git a/lldb/unittests/Host/JSONTransportTest.cpp b/lldb/unittests/Host/JSONTransportTest.cpp
index 2c26f94213773..3e977a70f5d4e 100644
--- a/lldb/unittests/Host/JSONTransportTest.cpp
+++ b/lldb/unittests/Host/JSONTransportTest.cpp
@@ -479,6 +479,15 @@ TEST_F(HTTPDelimitedJSONTransportTest, ReadWithEOF) {
   ASSERT_THAT_ERROR(Run(), Succeeded());
 }
 
+TEST_F(HTTPDelimitedJSONTransportTest, ReadWithEOFDestroyTransportOnClose) {
+  input.CloseWriteFileDescriptor();
+  EXPECT_CALL(message_handler, OnClosed()).WillOnce([this]() {
+    transport.reset();
+    loop.RequestTermination();
+  });
+  ASSERT_THAT_ERROR(loop.Run().takeError(), Succeeded());
+}
+
 TEST_F(HTTPDelimitedJSONTransportTest, ReaderWithUnhandledData) {
   std::string json = R"json({"str": "foo"})json";
   std::string message =
@@ -588,6 +597,15 @@ TEST_F(JSONRPCTransportTest, ReadWithEOF) {
   ASSERT_THAT_ERROR(Run(), Succeeded());
 }
 
+TEST_F(JSONRPCTransportTest, ReadWithEOFDestroyTransportOnClose) {
+  input.CloseWriteFileDescriptor();
+  EXPECT_CALL(message_handler, OnClosed()).WillOnce([this]() {
+    transport.reset();
+    loop.RequestTermination();
+  });
+  ASSERT_THAT_ERROR(loop.Run().takeError(), Succeeded());
+}
+
 TEST_F(JSONRPCTransportTest, ReaderWithUnhandledData) {
   std::string message = R"json({"req": "foo")json";
   // Write an incomplete message and close the handle.