diff --git a/pkg/domain/infra/abi/system_linux.go b/pkg/domain/infra/abi/system_linux.go
index 7acaa9bd19f..7c345aeed3b 100644
--- a/pkg/domain/infra/abi/system_linux.go
+++ b/pkg/domain/infra/abi/system_linux.go
@@ -4,6 +4,7 @@ package abi
 
 import (
 	"context"
+	"errors"
 	"fmt"
 	"os"
 
@@ -14,6 +15,7 @@ import (
 	"go.podman.io/common/pkg/config"
 	"go.podman.io/common/pkg/systemd"
 	"go.podman.io/storage/pkg/unshare"
+	"golang.org/x/sys/unix"
 )
 
 // Default path for system runtime state
@@ -59,6 +61,8 @@ func (ic *ContainerEngine) SetupRootless(_ context.Context, noMoveProcess bool,
 				}
 			}
 		}
+
+		// return early as we are already re-exec or root here so no need to join the rootless userns.
 		return nil
 	}
 
@@ -74,36 +78,41 @@ func (ic *ContainerEngine) SetupRootless(_ context.Context, noMoveProcess bool,
 	if became {
 		os.Exit(ret)
 	}
-	if noMoveProcess {
-		return nil
-	}
 
 	// if there is no pid file, try to join existing containers, and create a pause process.
 	ctrs, err := ic.Libpod.GetRunningContainers()
 	if err != nil {
-		logrus.Error(err.Error())
-		os.Exit(1)
+		return err
 	}
 
-	paths := []string{}
+	paths := make([]string, 0, len(ctrs))
 	for _, ctr := range ctrs {
 		paths = append(paths, ctr.ConfigNoCopy().ConmonPidFile)
 	}
 
 	if len(paths) > 0 {
 		became, ret, err = rootless.TryJoinFromFilePaths(pausePidPath, paths)
+		// TryJoinFromFilePaths fails with ESRCH when the PID are all not valid anymore
+		// In this case create a new userns.
+		if errors.Is(err, unix.ESRCH) {
+			logrus.Warnf("Failed to join existing conmon namespace, creating a new rootless podman user namespace. If there are existing container running please stop them with %q to reset the namespace", os.Args[0]+" system migrate")
+			became, ret, err = rootless.BecomeRootInUserNS(pausePidPath)
+		}
 	} else {
+		logrus.Info("Creating a new rootless user namespace")
 		became, ret, err = rootless.BecomeRootInUserNS(pausePidPath)
-		if err == nil {
-			systemd.MovePauseProcessToScope(pausePidPath)
-		}
 	}
+
 	if err != nil {
-		logrus.Error(fmt.Errorf("invalid internal status, try resetting the pause process with %q: %w", os.Args[0]+" system migrate", err))
-		os.Exit(1)
+		return fmt.Errorf("fatal error, invalid internal status, unable to create a new pause process: %w. Try running %q and if that doesn't work reboot to recover", err, os.Args[0]+" system migrate")
+	}
+	if !noMoveProcess {
+		systemd.MovePauseProcessToScope(pausePidPath)
 	}
 	if became {
 		os.Exit(ret)
 	}
+
+	logrus.Error("Internal error, failed to re-exec podman into user namespace without error. This should never happen, if you see this please report a bug")
 	return nil
 }
diff --git a/pkg/rootless/rootless_linux.c b/pkg/rootless/rootless_linux.c
index 3d74af6a6ca..644c8ef9a20 100644
--- a/pkg/rootless/rootless_linux.c
+++ b/pkg/rootless/rootless_linux.c
@@ -384,8 +384,7 @@ can_use_shortcut (char **argv)
           || strcmp (argv[argc], "version") == 0
           || strcmp (argv[argc], "context") == 0
           || strcmp (argv[argc], "search") == 0
-          || strcmp (argv[argc], "compose") == 0
-          || (strcmp (argv[argc], "system") == 0 && argv[argc+1] && strcmp (argv[argc+1], "service") != 0))
+          || strcmp (argv[argc], "compose") == 0)
         {
           ret = false;
           break;
diff --git a/test/system/550-pause-process.bats b/test/system/550-pause-process.bats
index da657e77e1c..7818f36bb9f 100644
--- a/test/system/550-pause-process.bats
+++ b/test/system/550-pause-process.bats
@@ -149,3 +149,30 @@ function _check_pause_process() {
     # This used to hang trying to unmount the netns.
     run_podman rm -f -t0 $cname
 }
+
+# regression test for https://issues.redhat.com/browse/RHEL-130252
+@test "podman system migrate works with conmon being killed" {
+    skip_if_not_rootless "pause process is only used as rootless"
+    skip_if_remote "system migrate not supported via remote"
+
+    local cname=c-$(safename)
+    run_podman run --name $cname --stop-signal SIGKILL -d $IMAGE sleep 100
+
+    run_podman inspect --format '{{.State.ConmonPid}}' $cname
+    conmon_pid="$output"
+
+    # check for pause pid and then kill it
+    _check_pause_process
+    kill -9 $pause_pid
+
+    # kill conmon
+    kill -9 $conmon_pid
+
+    # Use podman system migrate to stop the currently running pause process
+    run_podman 125 system migrate
+    assert "$output" =~ "Failed to join existing conmon namespace" "fallback to userns creating"
+    assert "$output" =~ "conmon process killed"
+
+    # Now the removal command should work fine without errors.
+    run_podman rm $cname
+}