diff --git a/spring-webmvc/src/main/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapter.java b/spring-webmvc/src/main/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapter.java
index adfea6246d92..d3e59c727766 100644
--- a/spring-webmvc/src/main/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapter.java
+++ b/spring-webmvc/src/main/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapter.java
@@ -1,5 +1,5 @@
 /*
- * Copyright 2002-2023 the original author or authors.
+ * Copyright 2002-2024 the original author or authors.
  *
  * Licensed under the Apache License, Version 2.0 (the "License");
  * you may not use this file except in compliance with the License.
@@ -95,6 +95,7 @@ public ModelAndView handle(HttpServletRequest servletRequest,
 			Object handler) throws Exception {
 
 		WebAsyncManager asyncManager = getWebAsyncManager(servletRequest, servletResponse);
+		servletResponse = getWrappedResponse(asyncManager);
 
 		ServerRequest serverRequest = getServerRequest(servletRequest);
 		ServerResponse serverResponse;
@@ -124,6 +125,22 @@ private WebAsyncManager getWebAsyncManager(HttpServletRequest servletRequest, Ht
 		return asyncManager;
 	}
 
+	/**
+	 * Obtain response wrapped by
+	 * {@link org.springframework.web.context.request.async.StandardServletAsyncWebRequest}
+	 * to enforce lifecycle rules from Servlet spec (section 2.3.3.4)
+	 * in case of async handling.
+	 */
+	private static HttpServletResponse getWrappedResponse(WebAsyncManager asyncManager) {
+		AsyncWebRequest asyncRequest = asyncManager.getAsyncWebRequest();
+		Assert.notNull(asyncRequest, "No AsyncWebRequest");
+
+		HttpServletResponse servletResponse = asyncRequest.getNativeResponse(HttpServletResponse.class);
+		Assert.notNull(servletResponse, "No HttpServletResponse");
+
+		return servletResponse;
+	}
+
 	private ServerRequest getServerRequest(HttpServletRequest servletRequest) {
 		ServerRequest serverRequest =
 				(ServerRequest) servletRequest.getAttribute(RouterFunctions.REQUEST_ATTRIBUTE);
diff --git a/spring-webmvc/src/test/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapterTests.java b/spring-webmvc/src/test/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapterTests.java
new file mode 100644
index 000000000000..555c45cdddfb
--- /dev/null
+++ b/spring-webmvc/src/test/java/org/springframework/web/servlet/function/support/HandlerFunctionAdapterTests.java
@@ -0,0 +1,107 @@
+/*
+ * Copyright 2002-2024 the original author or authors.
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *      https://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+package org.springframework.web.servlet.function.support;
+
+import java.io.IOException;
+import java.util.List;
+
+import jakarta.servlet.AsyncEvent;
+import jakarta.servlet.http.HttpServletResponse;
+import org.junit.jupiter.api.BeforeEach;
+import org.junit.jupiter.api.Test;
+
+import org.springframework.http.converter.StringHttpMessageConverter;
+import org.springframework.web.context.request.async.AsyncRequestNotUsableException;
+import org.springframework.web.context.request.async.StandardServletAsyncWebRequest;
+import org.springframework.web.context.request.async.WebAsyncManager;
+import org.springframework.web.context.request.async.WebAsyncUtils;
+import org.springframework.web.servlet.function.HandlerFunction;
+import org.springframework.web.servlet.function.RouterFunctions;
+import org.springframework.web.servlet.function.ServerRequest;
+import org.springframework.web.servlet.function.ServerResponse;
+import org.springframework.web.testfixture.servlet.MockAsyncContext;
+import org.springframework.web.testfixture.servlet.MockHttpServletRequest;
+import org.springframework.web.testfixture.servlet.MockHttpServletResponse;
+
+import static org.assertj.core.api.Assertions.assertThatThrownBy;
+import static org.mockito.BDDMockito.doThrow;
+import static org.mockito.BDDMockito.mock;
+
+/**
+ * Unit tests for {@link HandlerFunctionAdapter}.
+ *
+ * @author Rossen Stoyanchev
+ */
+public class HandlerFunctionAdapterTests {
+
+	private final MockHttpServletRequest servletRequest = new MockHttpServletRequest("GET", "/");
+
+	private final MockHttpServletResponse servletResponse = new MockHttpServletResponse();
+
+	private final HandlerFunctionAdapter adapter = new HandlerFunctionAdapter();
+
+
+	@BeforeEach
+	void setUp() {
+		this.servletRequest.setAttribute(RouterFunctions.REQUEST_ATTRIBUTE,
+				ServerRequest.create(this.servletRequest, List.of(new StringHttpMessageConverter())));
+	}
+
+
+	@Test
+	void asyncRequestNotUsable() throws Exception {
+
+		HandlerFunction<?> handler = request -> ServerResponse.sse(sseBuilder -> {
+			try {
+				sseBuilder.data("data 1");
+				sseBuilder.data("data 2");
+			}
+			catch (IOException ex) {
+				throw new RuntimeException(ex);
+			}
+		});
+
+		this.servletRequest.setAsyncSupported(true);
+
+		HttpServletResponse mockServletResponse = mock(HttpServletResponse.class);
+		doThrow(new IOException("Broken pipe")).when(mockServletResponse).getOutputStream();
+
+		// Use of response should be rejected
+		assertThatThrownBy(() -> adapter.handle(servletRequest, mockServletResponse, handler))
+				.hasRootCauseInstanceOf(IOException.class)
+				.hasRootCauseMessage("Broken pipe");
+	}
+
+	@Test
+	void asyncRequestNotUsableOnAsyncDispatch() throws Exception {
+
+		HandlerFunction<?> handler = request -> ServerResponse.ok().body("body");
+
+		// Put AsyncWebRequest in ERROR state
+		StandardServletAsyncWebRequest asyncRequest = new StandardServletAsyncWebRequest(servletRequest, servletResponse);
+		asyncRequest.onError(new AsyncEvent(new MockAsyncContext(servletRequest, servletResponse), new Exception()));
+
+		// Set it as the current AsyncWebRequest, from the initial REQUEST dispatch
+		WebAsyncManager asyncManager = WebAsyncUtils.getAsyncManager(servletRequest);
+		asyncManager.setAsyncWebRequest(asyncRequest);
+
+		// Use of response should be rejected
+		assertThatThrownBy(() -> adapter.handle(servletRequest, servletResponse, handler))
+				.isInstanceOf(AsyncRequestNotUsableException.class);
+	}
+
+}