diff --git a/zio-http/src/main/scala/zio/http/Route.scala b/zio-http/src/main/scala/zio/http/Route.scala
index 125389974a..2c6aa79e93 100644
--- a/zio-http/src/main/scala/zio/http/Route.scala
+++ b/zio-http/src/main/scala/zio/http/Route.scala
@@ -62,7 +62,8 @@ sealed trait Route[-Env, +Err] { self =>
     self match {
       case Provided(route, env)                     => Provided(route.handleErrorCause(f), env)
       case Augmented(route, aspect)                 => Augmented(route.handleErrorCause(f), aspect)
-      case Handled(routePattern, handler, location) => Handled(routePattern, handler, location)
+      case Handled(routePattern, handler, location) =>
+        Handled(routePattern, handler.mapErrorCause(c => f(c.asInstanceOf[Cause[Nothing]])), location)
 
       case Unhandled(rpm, handler, zippable, location) =>
         val handler2: Handler[Env, Response, Request, Response] = {
@@ -96,7 +97,8 @@ sealed trait Route[-Env, +Err] { self =>
     self match {
       case Provided(route, env)                     => Provided(route.handleErrorCauseZIO(f), env)
       case Augmented(route, aspect)                 => Augmented(route.handleErrorCauseZIO(f), aspect)
-      case Handled(routePattern, handler, location) => Handled(routePattern, handler, location)
+      case Handled(routePattern, handler, location) =>
+        Handled(routePattern, handler.mapErrorCauseZIO(c => f(c.asInstanceOf[Cause[Nothing]])), location)
 
       case Unhandled(rpm, handler, zippable, location) =>
         val handler2: Handler[Env, Response, Request, Response] = {
@@ -162,7 +164,14 @@ sealed trait Route[-Env, +Err] { self =>
     self match {
       case Provided(route, env)                     => Provided(route.handleErrorRequestCause(f), env)
       case Augmented(route, aspect)                 => Augmented(route.handleErrorRequestCause(f), aspect)
-      case Handled(routePattern, handler, location) => Handled(routePattern, handler, location)
+      case Handled(routePattern, handler, location) =>
+        Handled(
+          routePattern,
+          Handler.fromFunctionHandler[Request] { (req: Request) =>
+            handler.mapErrorCause(c => f(req, c.asInstanceOf[Cause[Nothing]]))
+          },
+          location,
+        )
 
       case Unhandled(rpm, handler, zippable, location) =>
         val handler2: Handler[Env, Response, Request, Response] = {
@@ -201,7 +210,14 @@ sealed trait Route[-Env, +Err] { self =>
     self match {
       case Provided(route, env)                     => Provided(route.handleErrorRequestCauseZIO(f), env)
       case Augmented(route, aspect)                 => Augmented(route.handleErrorRequestCauseZIO(f), aspect)
-      case Handled(routePattern, handler, location) => Handled(routePattern, handler, location)
+      case Handled(routePattern, handler, location) =>
+        Handled(
+          routePattern,
+          Handler.fromFunctionHandler[Request] { (req: Request) =>
+            handler.mapErrorCauseZIO(c => f(req, c.asInstanceOf[Cause[Nothing]]))
+          },
+          location,
+        )
 
       case Unhandled(rpm, handler, zippable, location) =>
         val handler2: Handler[Env, Response, Request, Response] = {
diff --git a/zio-http/src/test/scala/zio/http/RouteSpec.scala b/zio-http/src/test/scala/zio/http/RouteSpec.scala
index ab24e57f13..d1d4c02ea5 100644
--- a/zio-http/src/test/scala/zio/http/RouteSpec.scala
+++ b/zio-http/src/test/scala/zio/http/RouteSpec.scala
@@ -124,6 +124,46 @@ object RouteSpec extends ZIOHttpSpec {
           resultWarning == "error accessing /endpoint: hmm...",
         )
       },
+      test("handleErrorCause should handle defects") {
+        val route        = Method.GET / "endpoint" -> handler { (_: Request) => ZIO.dieMessage("hmm...") }
+        val errorHandled = route.handleErrorCause(_ => Response.text("error").status(Status.InternalServerError))
+        val request      = Request.get(URL.decode("/endpoint").toOption.get)
+        for {
+          response   <- errorHandled.toHttpApp.runZIO(request)
+          bodyString <- response.body.asString
+        } yield assertTrue(extractStatus(response) == Status.InternalServerError, bodyString == "error")
+      },
+      test("handleErrorCauseZIO should handle defects") {
+        val route        = Method.GET / "endpoint" -> handler { (_: Request) => ZIO.dieMessage("hmm...") }
+        val errorHandled =
+          route.handleErrorCauseZIO(_ => ZIO.succeed(Response.text("error").status(Status.InternalServerError)))
+        val request      = Request.get(URL.decode("/endpoint").toOption.get)
+        for {
+          response   <- errorHandled.toHttpApp.runZIO(request)
+          bodyString <- response.body.asString
+        } yield assertTrue(extractStatus(response) == Status.InternalServerError, bodyString == "error")
+      },
+      test("handleErrorRequestCause should handle defects") {
+        val route        = Method.GET / "endpoint" -> handler { (_: Request) => ZIO.dieMessage("hmm...") }
+        val errorHandled =
+          route.handleErrorRequestCause((_, _) => Response.text("error").status(Status.InternalServerError))
+        val request      = Request.get(URL.decode("/endpoint").toOption.get)
+        for {
+          response   <- errorHandled.toHttpApp.runZIO(request)
+          bodyString <- response.body.asString
+        } yield assertTrue(extractStatus(response) == Status.InternalServerError, bodyString == "error")
+      },
+      test("handleErrorRequestCauseZIO should handle defects") {
+        val route        = Method.GET / "endpoint" -> handler { (_: Request) => ZIO.dieMessage("hmm...") }
+        val errorHandled = route.handleErrorRequestCauseZIO((_, _) =>
+          ZIO.succeed(Response.text("error").status(Status.InternalServerError)),
+        )
+        val request      = Request.get(URL.decode("/endpoint").toOption.get)
+        for {
+          response   <- errorHandled.toHttpApp.runZIO(request)
+          bodyString <- response.body.asString
+        } yield assertTrue(extractStatus(response) == Status.InternalServerError, bodyString == "error")
+      },
     ),
   )
 }