diff --git a/main-actions/src/main/scala/sbt/internal/WorkerExchange.scala b/main-actions/src/main/scala/sbt/internal/WorkerExchange.scala
index fe22ca67c..eae02d416 100644
--- a/main-actions/src/main/scala/sbt/internal/WorkerExchange.scala
+++ b/main-actions/src/main/scala/sbt/internal/WorkerExchange.scala
@@ -24,8 +24,9 @@ import scala.sys.process.{ BasicIO, Process, ProcessIO }
 import scala.collection.mutable
 import scala.collection.concurrent.TrieMap
 import scala.collection.mutable.ListBuffer
-import scala.concurrent.{ Await, Promise }
+import scala.concurrent.{ Await, Future, Promise }
 import scala.concurrent.duration.*
+import scala.util.Try
 import scala.util.control.NonFatal
 
 object WorkerExchange:
@@ -83,11 +84,13 @@ object WorkerExchange:
       IO.classLocationPath(classOf[Gson]).toFile,
     )
     val inputRef = Promise[OutputStream]()
+    val responsesRead = Promise[Unit]()
     def runAccepter(out: OutputStream, in: InputStream): Unit =
       inputRef.success(out)
       val scanner = Scanner(in, "UTF-8")
       while scanner.hasNextLine() do notifyListeners(scanner.nextLine())
-    val (connArgs, closer): (Seq[String], Option[AutoCloseable]) = connectionType match
+      responsesRead.trySuccess(())
+    val (connArgs, closer) = connectionType match
       case WorkerConnection.Tcp =>
         val serverSocket = Retry(ServerSocket(0, 1, loopback))
         val accepter = Thread(() => {
@@ -130,20 +133,24 @@ object WorkerExchange:
     val onStdoutLine: String => Unit = connectionType match
       case WorkerConnection.Stdio => notifyListeners
       case _                      => (line) => scala.Console.out.println(line)
+    def readStdout(stdout: InputStream): Unit =
+      BasicIO.processFully(onStdoutLine)(stdout)
+      if connectionType == WorkerConnection.Stdio then responsesRead.trySuccess(())
     val processIo = ProcessIO(
       in = (input) =>
         (connectionType match
           case WorkerConnection.Stdio => inputRef.success(input)
           case _                      => ()
         ),
-      out = BasicIO.processFully(onStdoutLine),
+      out = readStdout,
       err = BasicIO.processFully((line) => scala.Console.err.println(line)),
     )
     val forkWithIo = fo.withOutputStrategy(OutputStrategy.CustomInputOutput(processIo))
     val p = Fork.java.fork(forkWithIo, options)
     val forkTimeout = fo.connectionTimeout.getOrElse(30.seconds)
     val input = Await.result(inputRef.future, forkTimeout)
-    WorkerProxy(input, p, options, closer)
+    WorkerProxy(input, p, options, closer, responsesRead.future)
+  end startWorker
 
   /** Generates a fresh path suitable for binding a `WorkerConnection.Ipc` socket. */
   def newIpcSocketPath(): NioPath =
@@ -178,6 +185,7 @@ class WorkerProxy(
     val process: Process,
     val options: Seq[String],
     closer: Option[AutoCloseable],
+    responsesRead: Future[Unit],
 ) extends AutoCloseable:
   lazy val inputStream = PrintStream(input)
   def close(): Unit =
@@ -194,11 +202,21 @@ class WorkerProxy(
 
   val watch = Thread(() => {
     while process.isAlive() do Thread.sleep(100)
+    Try(Await.ready(responsesRead, WorkerProxy.responseDrainTimeout))
     WorkerExchange.listeners.foreach(_.notifyExit(process))
   })
   watch.start()
 end WorkerProxy
 
+object WorkerProxy:
+  /**
+   * How long to keep reading a worker's responses after it exits, before reporting the exit.
+   * The reader reaches end of stream as soon as it has consumed everything the worker wrote;
+   * the bound only matters for a worker that died before connecting.
+   */
+  private val responseDrainTimeout = 10.seconds
+end WorkerProxy
+
 abstract class WorkerResponseListener extends Function1[String, Unit]:
   def notifyExit(p: Process): Unit
 
diff --git a/sbt-app/src/sbt-test/tests/fork-slow-listener/build.sbt b/sbt-app/src/sbt-test/tests/fork-slow-listener/build.sbt
new file mode 100644
index 000000000..9f889b515
--- /dev/null
+++ b/sbt-app/src/sbt-test/tests/fork-slow-listener/build.sbt
@@ -0,0 +1,11 @@
+scalaVersion := "3.9.0"
+Test / fork := true
+libraryDependencies += "org.scalameta" %% "munit" % "1.0.4" % Test
+
+Test / testListeners += new TestsListener:
+  def doInit(): Unit = ()
+  def startGroup(name: String): Unit = ()
+  def testEvent(event: TestEvent): Unit = Thread.sleep(50)
+  def endGroup(name: String, t: Throwable): Unit = ()
+  def endGroup(name: String, result: TestResult): Unit = ()
+  def doComplete(finalResult: TestResult): Unit = ()
diff --git a/sbt-app/src/sbt-test/tests/fork-slow-listener/src/test/scala/ManyTests.scala b/sbt-app/src/sbt-test/tests/fork-slow-listener/src/test/scala/ManyTests.scala
new file mode 100644
index 000000000..9f1ae0f39
--- /dev/null
+++ b/sbt-app/src/sbt-test/tests/fork-slow-listener/src/test/scala/ManyTests.scala
@@ -0,0 +1,2 @@
+class ManyTests extends munit.FunSuite:
+  (1 to 40).foreach(i => test(s"test $i")(assert(i < 40)))
diff --git a/sbt-app/src/sbt-test/tests/fork-slow-listener/test b/sbt-app/src/sbt-test/tests/fork-slow-listener/test
new file mode 100644
index 000000000..5a9f22365
--- /dev/null
+++ b/sbt-app/src/sbt-test/tests/fork-slow-listener/test
@@ -0,0 +1 @@
+-> test