diff --git a/build.sbt b/build.sbt
index e23addb45..81949a48c 100644
--- a/build.sbt
+++ b/build.sbt
@@ -1071,6 +1071,7 @@ lazy val mainProj = (project in file("main"))
       exclude[MissingClassProblem]("sbt.internal.server.BuildServerReporter$"),
       exclude[IncompatibleTemplateDefProblem]("sbt.internal.server.BuildServerReporter"),
       exclude[MissingClassProblem]("sbt.internal.CustomHttp*"),
+      exclude[ReversedMissingMethodProblem]("sbt.JobHandle.isAutoCancel"),
     )
   )
   .configure(
diff --git a/main/src/main/scala/sbt/BackgroundJobService.scala b/main/src/main/scala/sbt/BackgroundJobService.scala
index 6dc8deb81..62aaec76d 100644
--- a/main/src/main/scala/sbt/BackgroundJobService.scala
+++ b/main/src/main/scala/sbt/BackgroundJobService.scala
@@ -100,4 +100,5 @@ abstract class JobHandle {
   def id: Long
   def humanReadableName: String
   def spawningTask: ScopedKey[_]
+  def isAutoCancel: Boolean
 }
diff --git a/main/src/main/scala/sbt/Defaults.scala b/main/src/main/scala/sbt/Defaults.scala
index 1a8f61463..a86e7a0a1 100644
--- a/main/src/main/scala/sbt/Defaults.scala
+++ b/main/src/main/scala/sbt/Defaults.scala
@@ -2039,6 +2039,11 @@ object Defaults extends BuildCommon {
   def foregroundRunMainTask: Initialize[InputTask[Unit]] =
     Def.inputTask {
       val handle = bgRunMain.evaluated
+      handle match {
+        case threadJobHandle: AbstractBackgroundJobService#ThreadJobHandle =>
+          threadJobHandle.isAutoCancel = true
+        case _ =>
+      }
       val service = bgJobService.value
       service.waitForTry(handle).get
     }
@@ -2047,6 +2052,11 @@ object Defaults extends BuildCommon {
   def foregroundRunTask: Initialize[InputTask[Unit]] =
     Def.inputTask {
       val handle = bgRun.evaluated
+      handle match {
+        case threadJobHandle: AbstractBackgroundJobService#ThreadJobHandle =>
+          threadJobHandle.isAutoCancel = true
+        case _ =>
+      }
       val service = bgJobService.value
       service.waitForTry(handle).get
     }
diff --git a/main/src/main/scala/sbt/internal/DefaultBackgroundJobService.scala b/main/src/main/scala/sbt/internal/DefaultBackgroundJobService.scala
index ffce759d2..218cb3289 100644
--- a/main/src/main/scala/sbt/internal/DefaultBackgroundJobService.scala
+++ b/main/src/main/scala/sbt/internal/DefaultBackgroundJobService.scala
@@ -114,7 +114,8 @@ private[sbt] abstract class AbstractBackgroundJobService extends BackgroundJobSe
       override val spawningTask: ScopedKey[_],
       val logger: ManagedLogger,
       val workingDirectory: File,
-      val job: BackgroundJob
+      val job: BackgroundJob,
+      @volatile var isAutoCancel: Boolean = false,
   ) extends AbstractJobHandle {
     // EC for onStop handler below
     implicit val executionContext: ExecutionContext =
@@ -140,6 +141,7 @@ private[sbt] abstract class AbstractBackgroundJobService extends BackgroundJobSe
   private final class DeadHandle(override val id: Long, override val humanReadableName: String)
       extends AbstractJobHandle {
     override val spawningTask: ScopedKey[_] = unknownTask
+    override val isAutoCancel = false
   }
 
   def doRunInBackground(
@@ -513,7 +515,7 @@ private[sbt] object DefaultBackgroundJobService {
     backgroundJobServices
       .values()
       .forEach(jobService => {
-        jobService.jobs.foreach(jobService.stop)
+        jobService.jobs.filter(_.isAutoCancel).foreach(jobService.stop)
       })
   }