The Potters had looked like slowing their recent slide as Michael Kightly cancelled out an early Gabriel Agbonlahor effort.
But Lowton hit an unstoppable 30-yard volley to restore Villa's lead after 87 minutes and Benteke made sure of the points in injury time.
The victory will give Villa, having started the game in the bottom three, a huge lift but a crisis is growing for the Potters. Defeat left Pulis' men just one point above Villa and with only one win in 13 games.
Stoke looked up for the fight early on, but their optimism was pierced after just nine minutes as Lowton and Jordan Bowery combined from a throw-in to cut through the home defence.
Lowton reached the byline and pulled back for Agbonlahor, who rolled in at the second attempt after his initial effort was blocked.
The anxiety among the home fans was obvious and alarm bells were ringing again when Andreas Weimann broke clear and struck a post with a low shot Asmir Begovic may have brushed with his fingertips.
Stoke were booed off by a concerned crowd at half-time, but they had reason to cheer after the break when Jon Walters raced away down the left, fed inside to Charlie Adam and he turn teed up half-time substitute Kightly to stab home.
But the hosts were undone as Lowton dramatically swung the game back in Villa's favour with a superb volley three minutes from time. The defender chested down an attempted clearance from a corner outside the box and fired back into the top corner.
Home hopes were deflated and as the game ran towards injury time, Benteke raced through and calmly stroked the ball past Begovic for the third.