diff --git a/zio-http/src/main/scala/zio/http/netty/AsyncBodyReader.scala b/zio-http/src/main/scala/zio/http/netty/AsyncBodyReader.scala
index 55e752106f..5c481f7a31 100644
--- a/zio-http/src/main/scala/zio/http/netty/AsyncBodyReader.scala
+++ b/zio-http/src/main/scala/zio/http/netty/AsyncBodyReader.scala
@@ -16,6 +16,8 @@
 
 package zio.http.netty
 
+import java.io.IOException
+
 import zio.stacktracer.TracingImplicits.disableAutoTrace
 import zio.{Chunk, ChunkBuilder, Trace, Unsafe}
 
@@ -38,11 +40,22 @@ abstract class AsyncBodyReader(implicit trace: Trace) extends SimpleChannelInbou
     this.synchronized {
       state match {
         case State.Buffering =>
-          state = State.Direct(callback)
-          buffer.result().foreach { case (chunk, isLast) =>
-            callback(chunk, isLast)
+          val result: Chunk[(Chunk[Byte], Boolean)] = buffer.result()
+          val readingDone: Boolean                  = result.lastOption match {
+            case None              => false
+            case Some((_, isLast)) => isLast
           }
-          ctx.read()
+
+          if (ctx.channel.isOpen || readingDone) {
+            state = State.Direct(callback)
+            result.foreach { case (chunk, isLast) =>
+              callback(chunk, isLast)
+            }
+            ctx.read()
+          } else {
+            throw new IllegalStateException("Attempting to read from a closed channel, which will never finish")
+          }
+
         case State.Direct(_) =>
           throw new IllegalStateException("Cannot connect twice")
       }
@@ -91,6 +104,17 @@ abstract class AsyncBodyReader(implicit trace: Trace) extends SimpleChannelInbou
     }
     super.exceptionCaught(ctx, cause)
   }
+
+  override def channelInactive(ctx: ChannelHandlerContext): Unit = {
+    this.synchronized {
+      state match {
+        case State.Buffering        =>
+        case State.Direct(callback) =>
+          callback.fail(new IOException("Channel closed unexpectedly"))
+      }
+    }
+    ctx.fireChannelInactive()
+  }
 }
 
 object AsyncBodyReader {
diff --git a/zio-http/src/test/scala/zio/http/ClientSpec.scala b/zio-http/src/test/scala/zio/http/ClientSpec.scala
index f1a9eaef8b..8463f74598 100644
--- a/zio-http/src/test/scala/zio/http/ClientSpec.scala
+++ b/zio-http/src/test/scala/zio/http/ClientSpec.scala
@@ -86,6 +86,18 @@ object ClientSpec extends HttpRunnableSpec {
         loggedUrl <- ZTestLogger.logOutput.map(_.collectFirst { case m => m.annotations("url") }.mkString)
       } yield assertTrue(loggedUrl == s"$baseURL/")
     },
+    test("reading of unfinished body must fail") {
+      val app         = Handler.fromStream(ZStream.never).sandbox.toHttpApp
+      val requestCode = (client: Client) =>
+        (for {
+          response <- ZIO.scoped(client(Request()))
+          _        <- response.body.asStream.runForeach { _ => ZIO.succeed(0) }
+            .timeout(60.second) // timeout just in case it hangs
+        } yield ()).fold(success = _ => false, failure = _ => true)
+
+      val effect = app.deployAndRequest(requestCode).runZIO(())
+      assertZIO(effect)(isTrue)
+    },
   )
 
   override def spec = {
diff --git a/zio-http/src/test/scala/zio/http/internal/HttpRunnableSpec.scala b/zio-http/src/test/scala/zio/http/internal/HttpRunnableSpec.scala
index f493e75137..817bc8e395 100644
--- a/zio-http/src/test/scala/zio/http/internal/HttpRunnableSpec.scala
+++ b/zio-http/src/test/scala/zio/http/internal/HttpRunnableSpec.scala
@@ -55,9 +55,9 @@ abstract class HttpRunnableSpec extends ZIOHttpSpec { self =>
         }
       } yield response
 
-    def deployAndRequest(
-      call: Client => ZIO[Scope, Throwable, Response],
-    ): Handler[Client with DynamicServer with R with Scope, Throwable, Any, Response] =
+    def deployAndRequest[Output](
+      call: Client => ZIO[Scope, Throwable, Output],
+    ): Handler[Client with DynamicServer with R with Scope, Throwable, Any, Output] =
       for {
         port     <- Handler.fromZIO(DynamicServer.port)
         id       <- Handler.fromZIO(DynamicServer.deploy[R](app))