diff --git a/metals/src/main/scala/scala/meta/internal/metals/Messages.scala b/metals/src/main/scala/scala/meta/internal/metals/Messages.scala
index 317091cb03c..779636c0aa5 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/Messages.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/Messages.scala
@@ -585,31 +585,6 @@ object Messages {
       show = true,
     )
 
-  object DebugClassNotFound {
-
-    def invalidTargetClass(cls: String, target: String): MessageParams = {
-      new MessageParams(
-        MessageType.Error,
-        s"Class '$cls' not found in build target '$target'.",
-      )
-    }
-
-    def invalidTarget(target: String): MessageParams = {
-      new MessageParams(
-        MessageType.Error,
-        s"Target '$target' not found.",
-      )
-    }
-
-    def invalidClass(cls: String): MessageParams = {
-      new MessageParams(
-        MessageType.Error,
-        s"Class '$cls' not found.",
-      )
-    }
-
-  }
-
   object MissingScalafmtConf {
     def tryAgain(isAgain: Boolean): String =
       if (isAgain) ", try formatting again"
diff --git a/metals/src/main/scala/scala/meta/internal/metals/MetalsEnrichments.scala b/metals/src/main/scala/scala/meta/internal/metals/MetalsEnrichments.scala
index 0129b27ed2e..b31969117b4 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/MetalsEnrichments.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/MetalsEnrichments.scala
@@ -58,6 +58,8 @@ import com.google.gson.JsonObject
 import fansi.ErrorMode
 import io.undertow.server.HttpServerExchange
 import org.eclipse.lsp4j.TextDocumentIdentifier
+import org.eclipse.lsp4j.jsonrpc.ResponseErrorException
+import org.eclipse.lsp4j.jsonrpc.messages
 import org.eclipse.{lsp4j => l}
 
 /**
@@ -203,6 +205,17 @@ object MetalsEnrichments
     def asJavaObject: CompletableFuture[Object] =
       future.asJava.asInstanceOf[CompletableFuture[Object]]
 
+    def liftToLspError(implicit ec: ExecutionContext): Future[A] =
+      future.recoverWith { case NonFatal(e) =>
+        val newException = new ResponseErrorException(
+          new messages.ResponseError(
+            messages.ResponseErrorCode.InvalidRequest,
+            e.getMessage(),
+            null,
+          )
+        )
+        Future.failed(newException)
+      }
     def asJavaUnit(implicit ec: ExecutionContext): CompletableFuture[Unit] =
       future.ignoreValue.asJava
 
diff --git a/metals/src/main/scala/scala/meta/internal/metals/MetalsLspService.scala b/metals/src/main/scala/scala/meta/internal/metals/MetalsLspService.scala
index 26652e7088f..5d6a1359046 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/MetalsLspService.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/MetalsLspService.scala
@@ -1904,11 +1904,10 @@ class MetalsLspService(
   def analyzeStackTrace(content: String): Option[ExecuteCommandParams] =
     stacktraceAnalyzer.analyzeCommand(content)
 
-  def debugDiscovery(params: DebugDiscoveryParams): CompletableFuture[Object] =
+  def debugDiscovery(params: DebugDiscoveryParams): Future[DebugSession] =
     debugProvider
       .debugDiscovery(params)
       .flatMap(debugProvider.asSession)
-      .asJavaObject
 
   def findBuildTargetByDisplayName(target: String): Option[b.BuildTarget] =
     buildTargets.findByDisplayName(target)
diff --git a/metals/src/main/scala/scala/meta/internal/metals/WorkspaceLspService.scala b/metals/src/main/scala/scala/meta/internal/metals/WorkspaceLspService.scala
index def71ee16f9..799e019bf62 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/WorkspaceLspService.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/WorkspaceLspService.scala
@@ -23,8 +23,6 @@ import scala.meta.internal.metals.WindowStateDidChangeParams
 import scala.meta.internal.metals.clients.language.ConfiguredLanguageClient
 import scala.meta.internal.metals.clients.language.MetalsLanguageClient
 import scala.meta.internal.metals.config.StatusBarState
-import scala.meta.internal.metals.debug.BuildTargetNotFoundException
-import scala.meta.internal.metals.debug.BuildTargetUndefinedException
 import scala.meta.internal.metals.debug.DebugProvider
 import scala.meta.internal.metals.doctor.DoctorVisibilityDidChangeParams
 import scala.meta.internal.metals.doctor.HeadDoctor
@@ -93,6 +91,7 @@ import org.eclipse.lsp4j.TextDocumentPositionParams
 import org.eclipse.lsp4j.TextEdit
 import org.eclipse.lsp4j.WorkspaceEdit
 import org.eclipse.lsp4j.WorkspaceSymbolParams
+import org.eclipse.lsp4j.jsonrpc.ResponseErrorException
 import org.eclipse.lsp4j.jsonrpc.messages
 
 class WorkspaceLspService(
@@ -639,10 +638,20 @@ class WorkspaceLspService(
       folderServices.foreach(_.pause())
     }
 
-  private def displayNotFound(objectName: String, id: String) =
-    languageClient.showMessage(
-      Messages.errorMessageParams(s"$objectName not found: $id")
-    )
+  private def failedRequest(
+      message: String
+  ): Future[Object] = {
+    Future
+      .failed(
+        new ResponseErrorException(
+          new messages.ResponseError(
+            messages.ResponseErrorCode.InvalidParams,
+            message,
+            null,
+          )
+        )
+      )
+  }
 
   private def onFirstSatifying[T, R](mapTo: MetalsLspService => Future[T])(
       satisfies: T => Boolean,
@@ -842,21 +851,16 @@ class WorkspaceLspService(
         ) match {
           case Some(service) => service.startDebugProvider(params).asJavaObject
           case None =>
-            languageClient.showMessage(
-              Messages.errorMessageParams(
-                s"Could not find folder for build targets: ${targets.mkString(",")}"
-              )
-            )
-            Future.failed(DebugProvider.WorkspaceErrorsException).asJavaObject
+            failedRequest(
+              s"Could not find folder for build targets: ${targets.mkString(",")}"
+            ).asJavaObject
         }
       case ServerCommands.StartMainClass(params) if params.mainClass != null =>
         DebugProvider
           .getResultFromSearches(
             folderServices.map(_.mainClassSearch(params))
-          ) {
-            displayNotFound("Main class", params.mainClass)
-            Future.failed(new ju.NoSuchElementException(params.mainClass))
-          }
+          )
+          .liftToLspError
           .asJavaObject
 
       case ServerCommands.StartTestSuite(params)
@@ -867,20 +871,15 @@ class WorkspaceLspService(
           _.isDefined,
           (service, someTarget) =>
             service.startTestSuite(someTarget.get, params),
-          () => {
-            displayNotFound("Build target", params.target.toString())
-            Future.failed(BuildTargetNotFoundException(params.target.getUri))
-          },
+          () => failedRequest(s"Could not find '${params.target}' build target"),
         ).asJavaObject
       case ServerCommands.ResolveAndStartTestSuite(params)
           if params.testClass != null =>
         DebugProvider
           .getResultFromSearches(
             folderServices.map(_.testClassSearch(params))
-          ) {
-            displayNotFound("Test class", params.testClass)
-            Future.failed(new ju.NoSuchElementException(params.testClass))
-          }
+          )
+          .liftToLspError
           .asJavaObject
       case ServerCommands.StartAttach(params) if params.hostName != null =>
         onFirstSatifying(service =>
@@ -891,13 +890,16 @@ class WorkspaceLspService(
           _.isDefined,
           (service, someTarget) =>
             service.createDebugSession(someTarget.get.getId()),
-          () => {
-            displayNotFound("Build target", params.buildTarget)
-            Future.failed(BuildTargetUndefinedException())
-          },
+          () =>
+            failedRequest(
+              s"Could not find '${params.buildTarget}' build target"
+            ),
         ).asJavaObject
       case ServerCommands.DiscoverAndRun(params) =>
-        getServiceFor(params.path).debugDiscovery(params)
+        getServiceFor(params.path)
+          .debugDiscovery(params)
+          .liftToLspError
+          .asJavaObject
       case ServerCommands.AnalyzeStacktrace(content) =>
         Future {
           // Getting the service for focused document and first one otherwise
diff --git a/metals/src/main/scala/scala/meta/internal/metals/debug/BuildTargetClassesFinder.scala b/metals/src/main/scala/scala/meta/internal/metals/debug/BuildTargetClassesFinder.scala
index 1d13cd66872..11931f706f2 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/debug/BuildTargetClassesFinder.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/debug/BuildTargetClassesFinder.scala
@@ -39,8 +39,9 @@ class BuildTargetClassesFinder(
         // We check whether there is a main in dependencies that is not reported via BSP
         case ClassNotFoundInBuildTargetException(className, target) =>
           revertToDependencies(className, Some(target))
-        case _: ClassNotFoundException =>
+        case _: NoClassFoundException =>
           revertToDependencies(className, buildTarget = None)
+        case _ => Nil
       }
       found match {
         case Nil => Failure(ex)
@@ -109,7 +110,7 @@ class BuildTargetClassesFinder(
           }
           .reverse
       if (classes.nonEmpty) Success(classes)
-      else Failure(new ClassNotFoundException(className))
+      else Failure(new NoClassFoundException(className))
     } { targetName =>
       buildTargets
         .findByDisplayName(targetName)
@@ -148,15 +149,19 @@ class BuildTargetClassesFinder(
 case class BuildTargetNotFoundException(buildTargetName: String)
     extends Exception(s"Build target not found: $buildTargetName")
 
-case class BuildTargetUndefinedException()
-    extends Exception("Debugger configuration is missing 'buildTarget' param.")
-
 case class ClassNotFoundInBuildTargetException(
     className: String,
     buildTarget: b.BuildTarget,
 ) extends Exception(
       s"Class '$className' not found in build target '${buildTarget.getDisplayName()}'"
     )
+
+case class NoClassFoundException(
+    className: String
+) extends Exception(
+      s"Class '$className' not found in any build target"
+    )
+
 case class BuildTargetNotFoundForPathException(path: AbsolutePath)
     extends Exception(
       s"No build target could be found for the path: ${path.toString()}"
diff --git a/metals/src/main/scala/scala/meta/internal/metals/debug/DebugProvider.scala b/metals/src/main/scala/scala/meta/internal/metals/debug/DebugProvider.scala
index d97b8199217..2022b56bef6 100644
--- a/metals/src/main/scala/scala/meta/internal/metals/debug/DebugProvider.scala
+++ b/metals/src/main/scala/scala/meta/internal/metals/debug/DebugProvider.scala
@@ -688,40 +688,6 @@ class DebugProvider(
       languageClient.metalsStatus(
         Messages.DebugErrorsPresent(clientConfig.icons())
       )
-    case t: ClassNotFoundException =>
-      languageClient.showMessage(
-        Messages.DebugClassNotFound.invalidClass(t.getMessage())
-      )
-    case ClassNotFoundInBuildTargetException(cls, buildTarget) =>
-      languageClient.showMessage(
-        Messages.DebugClassNotFound
-          .invalidTargetClass(cls, buildTarget.getDisplayName())
-      )
-    case BuildTargetNotFoundException(target) =>
-      languageClient.showMessage(
-        Messages.DebugClassNotFound
-          .invalidTarget(target)
-      )
-    case e: BuildTargetNotFoundForPathException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
-    case e: BuildTargetContainsNoMainException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
-    case e: BuildTargetUndefinedException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
-    case e: NoTestsFoundException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
-    case e: RunType.UnknownRunTypeException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
     case e @ SemanticDbNotFoundException =>
       languageClient.metalsStatus(
         MetalsStatusParams(
@@ -730,13 +696,7 @@ class DebugProvider(
           command = ClientCommands.RunDoctor.id,
         )
       )
-    case e @ DotEnvFileParser.InvalidEnvFileException(_) =>
-      languageClient.showMessage(Messages.errorMessageParams(e.getMessage()))
-
-    case e @ NoRunOptionException =>
-      languageClient.showMessage(
-        Messages.errorMessageParams(e.getMessage())
-      )
+    case _ =>
   }
 
   private def parseSessionName(
@@ -829,7 +789,7 @@ class DebugProvider(
           _ <- buildTargetClasses.rebuildIndex(target)
           result <- Future(f())
         } yield result
-      case Failure(_: ClassNotFoundException) =>
+      case Failure(_: NoClassFoundException) =>
         val allTargetIds = buildTargets.allBuildTargetIds
         for {
           _ <- compilations.compileTargets(allTargetIds)
@@ -867,6 +827,26 @@ class DebugProvider(
 
 object DebugProvider {
 
+  private def exceptionOrder(t: Throwable): Int = t match {
+    /* Validation errors, should shown first as they are relevant for each build target.
+     */
+    case DotEnvFileParser.InvalidEnvFileException(_) => 0
+    case NoRunOptionException => 1
+    case _: RunType.UnknownRunTypeException => 2
+    /* Target found, but class not, means that we managed to find the proper workspace folder
+     */
+    case _: ClassNotFoundInBuildTargetException => 3
+    case _: BuildTargetContainsNoMainException => 4
+    case _: NoTestsFoundException => 5
+    /* These exception will show up and it's hard to pinpoint which folder we should be in
+     * since we failed to fin the exception anywhere. Probably just showing the error is enough.
+     */
+    case _: BuildTargetNotFoundForPathException => 6
+    case _: NoClassFoundException => 7
+    case _: BuildTargetNotFoundException => 8
+    case _ => 9
+  }
+
   /**
    * Given an occurence and a text document return the symbol of a main method
    * that could be defined using the Scala 3 @main annotation.
@@ -958,16 +938,16 @@ object DebugProvider {
     protected def dapSessionParams(res: A): Future[DebugSessionParams]
     def createDapSession(args: A): Future[DebugSession] =
       dapSessionParams(args).flatMap(debugProvider.asSession(_))
-    def searchResult: Future[(Option[A], ClassSearch[A])] = {
+    def searchResult: Future[(Try[A], ClassSearch[A])] = {
       Future {
         val resolved = search()
         searchPromise.trySuccess(resolved)
       }
-      searchPromise.future.map(e => (e.toOption, this))
+      searchPromise.future.map(e => (e, this))
     }
-    def retrySearchResult: Future[(Option[A], ClassSearch[A])] =
+    def retrySearchResult: Future[(Try[A], ClassSearch[A])] =
       searchPromise.future
-        .flatMap(debugProvider.retryAfterRebuild(_, search).map(_.toOption))
+        .flatMap(debugProvider.retryAfterRebuild(_, search))
         .map((_, this))
   }
 
@@ -1000,27 +980,32 @@ object DebugProvider {
       debugProvider.buildTestClassParams(res, params)
   }
 
-  def getResultFromSearches[A](searches: List[ClassSearch[A]])(
-      default: => Future[DebugSession]
+  def getResultFromSearches[A](
+      searches: List[ClassSearch[A]]
   )(implicit ec: ExecutionContext): Future[DebugSession] =
     Future
       .sequence(searches.map(_.searchResult))
-      .getFirstOrElse(
-        Future
-          .sequence(searches.map(_.retrySearchResult))
-          .getFirstOrElse(default)
-      )
+      .getFirstOrError
+      .recoverWith { case _ =>
+        Future.sequence(searches.map(_.retrySearchResult)).getFirstOrError
+      }
 
   private implicit class FindFirstDebugSession[A](
-      from: Future[List[(Option[A], ClassSearch[A])]]
+      from: Future[List[(Try[A], ClassSearch[A])]]
   ) {
-    def getFirstOrElse(
-        default: => Future[DebugSession]
-    )(implicit ec: ExecutionContext): Future[DebugSession] =
-      from.flatMap {
-        _.collectFirst { case (Some(dapSession), search) =>
-          search.createDapSession(dapSession)
-        }.getOrElse(default)
+    def getFirstOrError(implicit ec: ExecutionContext): Future[DebugSession] =
+      from.flatMap { all =>
+        def mostRelevantError() = all
+          .collect { case (Failure(error), _) =>
+            error
+          }
+          .sortBy(DebugProvider.exceptionOrder)
+          .head
+        all
+          .collectFirst { case (Success(dapSession), search) =>
+            search.createDapSession(dapSession)
+          }
+          .getOrElse(Future.failed(mostRelevantError()))
       }
   }
 }
diff --git a/tests/unit/src/test/scala/tests/DebugDiscoverySuite.scala b/tests/unit/src/test/scala/tests/DebugDiscoverySuite.scala
index a5d7391649c..22a25d697be 100644
--- a/tests/unit/src/test/scala/tests/DebugDiscoverySuite.scala
+++ b/tests/unit/src/test/scala/tests/DebugDiscoverySuite.scala
@@ -12,6 +12,8 @@ import scala.meta.internal.metals.debug.DotEnvFileParser.InvalidEnvFileException
 import scala.meta.internal.metals.debug.NoTestsFoundException
 import scala.meta.io.AbsolutePath
 
+import org.eclipse.lsp4j.jsonrpc.ResponseErrorException
+
 // note(@tgodzik) all test have `System.exit(0)` added to avoid occasional issue due to:
 // https://stackoverflow.com/questions/2225737/error-jdwp-unable-to-get-jni-1-2-environment
 class DebugDiscoverySuite
@@ -148,10 +150,10 @@ class DebugDiscoverySuite
             "runOrTestFile",
           ).toJson
         )
-        .recover { case e @ DebugProvider.NoRunOptionException => e }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString(),
-      DebugProvider.NoRunOptionException.toString(),
+      DebugProvider.NoRunOptionException.getMessage(),
     )
   }
 
@@ -215,12 +217,10 @@ class DebugDiscoverySuite
             "run",
           ).toJson
         )
-        .recover { case e: BuildTargetContainsNoMainException =>
-          e
-        }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString,
-      BuildTargetContainsNoMainException("a").toString(),
+      BuildTargetContainsNoMainException("a").getMessage(),
     )
   }
 
@@ -247,12 +247,10 @@ class DebugDiscoverySuite
             "run",
           ).toJson
         )
-        .recover { case WorkspaceErrorsException =>
-          WorkspaceErrorsException
-        }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString,
-      WorkspaceErrorsException.toString(),
+      WorkspaceErrorsException.getMessage(),
     )
   }
 
@@ -324,10 +322,10 @@ class DebugDiscoverySuite
             envFile = fakePath,
           ).toJson
         )
-        .recover { case e: InvalidEnvFileException => e }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString,
-      InvalidEnvFileException(AbsolutePath(fakePath)).toString(),
+      InvalidEnvFileException(AbsolutePath(fakePath)).getMessage(),
     )
   }
 
@@ -426,10 +424,10 @@ class DebugDiscoverySuite
             "testTarget",
           ).toJson
         )
-        .recover { case e: NoTestsFoundException => e }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString(),
-      NoTestsFoundException("build target", "a").toString(),
+      NoTestsFoundException("build target", "a").getMessage(),
     )
   }
 
@@ -460,12 +458,10 @@ class DebugDiscoverySuite
             "testFile",
           ).toJson
         )
-        .recover { case SemanticDbNotFoundException =>
-          SemanticDbNotFoundException
-        }
+        .recover { case e: ResponseErrorException => e.getMessage }
     } yield assertNoDiff(
       result.toString,
-      SemanticDbNotFoundException.toString(),
+      SemanticDbNotFoundException.getMessage(),
     )
   }
 }
diff --git a/tests/unit/src/test/scala/tests/DebugProtocolSuite.scala b/tests/unit/src/test/scala/tests/DebugProtocolSuite.scala
index 43505140713..5cc9e4abd37 100644
--- a/tests/unit/src/test/scala/tests/DebugProtocolSuite.scala
+++ b/tests/unit/src/test/scala/tests/DebugProtocolSuite.scala
@@ -16,6 +16,7 @@ import scala.meta.internal.metals.debug.DebugProvider.WorkspaceErrorsException
 
 import ch.epfl.scala.bsp4j.DebugSessionParamsDataKind
 import ch.epfl.scala.bsp4j.ScalaMainClass
+import org.eclipse.lsp4j.jsonrpc.ResponseErrorException
 
 // note(@tgodzik) all test have `System.exit(0)` added to avoid occasional issue due to:
 // https://stackoverflow.com/questions/2225737/error-jdwp-unable-to-get-jni-1-2-environment
@@ -410,12 +411,12 @@ class DebugProtocolSuite
               singletonList("Foo"),
             ).toJson
           )
-          .recover { case WorkspaceErrorsException =>
-            WorkspaceErrorsException
+          .recover { case e: ResponseErrorException =>
+            e.getMessage()
           }
-    } yield assertDiffEqual(
+    } yield assertNoDiff(
       result.toString(),
-      WorkspaceErrorsException.toString(),
+      WorkspaceErrorsException.getMessage(),
     )
   }
 
@@ -484,12 +485,12 @@ class DebugProtocolSuite
               "a.Foo"
             ).toJson
           )
-          .recover { case WorkspaceErrorsException =>
-            WorkspaceErrorsException
+          .recover { case e: ResponseErrorException =>
+            e.getMessage()
           }
-    } yield assertContains(
+    } yield assertNoDiff(
       result.toString(),
-      WorkspaceErrorsException.toString(),
+      WorkspaceErrorsException.getMessage(),
     )
   }
 }