diff --git a/main/src/main/scala/sbt/plugins/SemanticdbPlugin.scala b/main/src/main/scala/sbt/plugins/SemanticdbPlugin.scala
index f0e478542..8fcd295ed 100644
--- a/main/src/main/scala/sbt/plugins/SemanticdbPlugin.scala
+++ b/main/src/main/scala/sbt/plugins/SemanticdbPlugin.scala
@@ -18,6 +18,7 @@ import sbt.librarymanagement.{ Configuration, CrossVersion }
 import ProjectExtra.inConfig
 import sbt.internal.inc.ScalaInstance
 import sbt.ScopeFilter.Make.*
+import sbt.util.CacheImplicits.given
 
 object SemanticdbPlugin extends AutoPlugin {
   override def requires = JvmPlugin
@@ -54,6 +55,10 @@ object SemanticdbPlugin extends AutoPlugin {
     inConfig(Test)(configurationSettings)
 
   lazy val configurationSettings: Seq[Def.Setting[?]] = List(
+    compileIncremental := Def.taskIf {
+      if (semanticdbIncludeInJar.value || !semanticdbEnabled.value) compileIncremental.value
+      else compileIncAndCacheSemanticdbTargetRootTask.value
+    }.value,
     semanticdbTargetRoot := {
       val converter = fileConverter.value
       val in = semanticdbIncludeInJar.value
@@ -93,6 +98,16 @@ object SemanticdbPlugin extends AutoPlugin {
     }
   }
 
+  private val compileIncAndCacheSemanticdbTargetRootTask = Def.cachedTask {
+    val prev = compileIncremental.value
+    val converter = fileConverter.value
+    val targetRoot = semanticdbTargetRoot.value
+
+    val vfTargetRoot = converter.toVirtualFile(targetRoot.toPath)
+    Def.declareOutputDirectory(vfTargetRoot)
+    prev
+  }
+
   private def ancestorConfigs(config: Configuration) = {
     def ancestors(configs: Vector[Configuration]): Vector[Configuration] =
       configs ++ configs.flatMap(conf => ancestors(conf.extendsConfigs))
diff --git a/sbt-app/src/sbt-test/actions/compile-time-only/build.sbt b/sbt-app/src/sbt-test/actions/compile-time-only/build.sbt
index e4ebcd167..99ce64624 100644
--- a/sbt-app/src/sbt-test/actions/compile-time-only/build.sbt
+++ b/sbt-app/src/sbt-test/actions/compile-time-only/build.sbt
@@ -5,7 +5,7 @@ lazy val expectErrorNotCrash = taskKey[Unit]("Ensures that sbt properly set type
 
 expectErrorNotCrash := {
   val fail = (Compile / compileIncremental).failure.value
-  fail.directCause match
+  Incomplete.allExceptions(fail).headOption match
     case Some(x: xsbti.CompileFailed) => ()
     case _ => sys.error("Compiler crashed instead of providing a compile-time-only exception.")
 }
diff --git a/sbt-app/src/sbt-test/project/semanticdbEnabled/build.sbt b/sbt-app/src/sbt-test/project/semanticdbEnabled/build.sbt
new file mode 100644
index 000000000..3bd26a503
--- /dev/null
+++ b/sbt-app/src/sbt-test/project/semanticdbEnabled/build.sbt
@@ -0,0 +1,10 @@
+semanticdbEnabled := true
+
+val matrix = projectMatrix
+  .defaultAxes(VirtualAxis.jvm)
+  .jvmPlatform(scalaVersions =
+    Seq(
+      "2.12.20", // semanticdb support via semanticdb-scalac
+      "3.6.4" // built-in semanticdb support
+    )
+  )
diff --git a/sbt-app/src/sbt-test/project/semanticdbEnabled/matrix/src/main/scala/foo/Compile.scala b/sbt-app/src/sbt-test/project/semanticdbEnabled/matrix/src/main/scala/foo/Compile.scala
new file mode 100644
index 000000000..fdd81fb04
--- /dev/null
+++ b/sbt-app/src/sbt-test/project/semanticdbEnabled/matrix/src/main/scala/foo/Compile.scala
@@ -0,0 +1,7 @@
+package foo
+
+object Compile {
+  def main(args: Array[String]): Unit = {
+    println("hello world")
+  }
+}
diff --git a/sbt-app/src/sbt-test/project/semanticdbEnabled/test b/sbt-app/src/sbt-test/project/semanticdbEnabled/test
new file mode 100644
index 000000000..d397c7b1d
--- /dev/null
+++ b/sbt-app/src/sbt-test/project/semanticdbEnabled/test
@@ -0,0 +1,25 @@
+> compile
+$ exists target/**/scala-2.12*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+$ exists target/**/scala-3*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+
+> clean
+-$ exists target/**/scala-2.12*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+-$ exists target/**/scala-3*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+> compile
+$ exists target/**/scala-2.12*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+$ exists target/**/scala-3*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+
+> set LocalProject("matrix2_12") / Compile / semanticdbTargetRoot := (LocalProject("matrix2_12") / Compile / target).value / "custom212"
+> set LocalProject("matrix3") / Compile / semanticdbTargetRoot := (LocalProject("matrix3") / Compile / target).value / "custom3"
+
+> compile
+$ exists target/**/scala-2.12*/**/custom212/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+$ exists target/**/scala-3*/**/custom3/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+
+> clean
+> compile
+-$ exists target/**/scala-2.12*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+-$ exists target/**/scala-3*/**/meta/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+$ exists target/**/scala-2.12*/**/custom212/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+$ exists target/**/scala-3*/**/custom3/META-INF/semanticdb/matrix/src/main/scala/foo/Compile.scala.semanticdb
+