Former Stoke boss Alex Neil saw Millwall move back into the Championship top two and guarantee a play-off place with a 3-1 win at the bet365 Stadium.
Camiel Neghli fired the Londoners into a first-half lead before Femi Azeez's ninth goal of the season made it 2-0 after 55 minutes.
A Caleb Taylor own goal on the hour made Neil and his team sweat before Josh Coburn wrapped up the points with a 69th-minute strike, punishing some sloppy home defending.
Millwall's win lifted them three points above third-placed Ipswich, who travel to Charlton on Wednesday.
Stoke, whose season of promise is fading rapidly with only two wins now from their last 10 games, handed first starts to academy duo Pijus Otegbayo and fellow 18-year-old defender Syd Agina.
The Potters almost took a 12th-minute lead but Anthony Patterson smartly turned away a shot from Robert Bozenik, making his first start since January 1.
Millwall quickly countered and Coburn missed his first chance of the night after an inviting cross from Tristan Crama.
Neghli, however, showed him how to finish after 20 minutes, netting for a second successive match.
Zak Sturge provided the opportunity with a teasing centre from the left and when Eric Bocat couldn't sort out his feet to clear, Neghli curled in a superb rising left-foot drive.
It should have been two four minutes later. This time Neghli turned provider but Coburn contrived to blaze over from seven yards.
Four minutes from half-time, Crama's misplaced pass provided an unexpected chance for Lewis Baker but on-loan Sunderland keeper Patterson was equal to the City skipper's 25-yarder.
Patterson was beaten after 48 minutes but his right-hand upright kept out Tatsuki Seko's volley after Millwall failed to clear Baker's corner.
Stoke kept up the pressure and Patterson intervened to deny Million Manhoef.
There was relief among the 1,302 travelling fans when Azeez doubled the Lions' advantage.
There looked little danger when the highly-prized winger picked up a pass just outside the penalty area but his fiercely-struck left-foot shot proved too hot to handle for keeper Gavin Bazunu.
Stoke hit back immediately with the aid of a slice of luck.
With his first touch, substitute Lamine Cisse dinked a ball into the six-yard box and Taylor's unintentional touch wrong-footed Patterson.
But Coburn made it third time lucky after Bocat gifted the ball to Neghli to claim his 10th goal of the season.
Stoke's Mark Robins:
"I am sick of teams who come here and look ordinary and take the points.
"This is a team going for automatic promotion so it gives me loads of food for thought.
"It has been poor for a while. Summer can't come soon enough, that's for sure.
"There are too many at the moment choosing not to give everything. I have got plenty to do.
"It was not good enough so you have to change things and change the way you go about it.
"It is a season that promised so much at the start and has delivered nothing. It is really difficult to get excited about.
"In the interim we have had decent performances in a season that hasn't panned out to the level we wanted it to."
Millwall's Alex Neil:
"We will fight to the end and see where it takes us.
"It is the biggest achievement the club has had in the last 24 or 25 years and we still have two games to play.
"We have our eye on what the next two games look like. We need to try and win those games and let's see what happens elsewhere.
"The fact we are in the fight for automatic promotion is an incredible achievement for this team, this club and everyone connected with it.
"If we end up in the play-offs we will give it our best shot. There is so much to like about this team and I'm privileged I have this opportunity to coach them.
"For us to be on 79 points (Millwall's second highest second-tier tally) with two games remaining has been a dream season for us in terms of what our expectations would have been."
