Ronaldo equalised for United after Van Nistelrooy's mis-hit shot
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Wigan defender Pascal Chimbonda scored a desperately unlucky own goal to hand Manchester United a last-gasp victory.
The Latics, soundly beaten by United in the Carling Cup final eight days ago, dominated the first half and led after an hour through Paul Scharner's tap-in.
United equalised when shock substitute Ruud van Nistelrooy's mis-hit shot set up team-mate Cristiano Ronaldo.
Then at the death, Louis Saha's deflected shot hit the bar and ricocheted into the net off Chimbonda.
The three points moved a jubilant United back above Liverpool into second in the Premiership table, but it was an agonising end for Wigan, whose two previous meetings with United this season had both ended in 4-0 defeats.
Van Nistelrooy, also left out of Sir Alex Ferguson's Carling Cup team, started the game on the bench and looked a forlorn figure.
But even he would have found chances hard to come by in a vibrant first half from the hosts, who made their mark early.
Ronaldo, who upset Wigan by showboating as United coasted to victory in the Carling Cup, was floored within five minutes by a late tackle from Arjan de Zeeuw.
The Wigan skipper was deservedly booked, but the incident seemed to embolden his side, with strikers Jason Roberts and Henri Camara consistently troubling Rio Ferdinand and Wes Brown at the heart of United's defence.
Camara created the game's first clear chance after seven minutes, setting up Gary Teale, who scooped his shot over the bar.
Camara then found Roberts with a header, but his striker partner nodded the ball straight at Edwin van der Sar from three yards out.
United were on the back foot but still could have taken the lead when a sweet move featuring Ronaldo ended with Wayne Rooney overhitting a pass to Saha when he might have shot.
Wigan were quickly back on the attack, Camara slicing wide from Lee McCulloch's flick-on and Graham Kavanagh twice sending Van der Sar scrambling with sweetly-struck volleys.
The only disappointment for the home side at the break was their failure to convert their chances - and they were almost made to pay three minutes into the second half.
Gary Neville galloped into space on the right and crossed for Rooney, who headed well over from a good position.
But just as United looked like they might have weathered the Wigan storm, the hosts pounced from a corner.
Ryan Giggs cleared De Zeeuw's header off the line and Van der Sar blocked Roberts' follow-up but the ball eventually fell to an unmarked Scharner, who gleefully tapped in.
Ferguson responded by introducing Van Nistelrooy - and the Dutchman, albeit accidentally, made an immediate impact when his miskick fell to Ronaldo, who slotted home.
If the equaliser seemed like rough justice for the home side, the winner was harsh.
John Filan smothered Saha's shot, but it came back off the bar, hit Chimbonda and bounced agonisingly into the net - despite the Wigan defender's frantic efforts to stop it.
Wigan boss Paul Jewell:
"It was a poxy goal to lose to.
"We don't want people to feel sorry for us. I'm sick for the players and fans - you could see by how United celebrated that they felt they got out of jail.
"We played well but lady luck was just against us. I can't ask for any more effort and we pushed them all the way."
Manchester United manager Sir Alex Ferguson:
"I don't think we've had a harder away game all season - Wigan were brilliant, absolutely terrific.
"They didn't deserve to lose - it was so unlucky for Pascal Chimbonda, he couldn't do much about it in the end.
"We were poor in the first half but we improved and then gambled. I'd have settled for 1-1 as they were so good."
Wigan: Filan, Chimbonda, Scharner, De Zeeuw, Baines, Teale, Bullard, Kavanagh, McCulloch (Ziegler 89), Roberts, Camara.
Subs Not Used: Walsh, Jackson, Johansson, Thompson.
Booked: De Zeeuw, Kavanagh, Scharner, McCulloch, Baines.
Goals: Scharner 60.
Man Utd: Van der Sar, Neville, Ferdinand, Brown, Silvestre (Evra 85), Ronaldo, O'Shea, Giggs, Park (van Nistelrooy 71), Saha, Rooney.
Subs Not Used: Howard, Vidic, Richardson.
Booked: Giggs, O'Shea, Neville.
Goals: Ronaldo 74, Chimbonda 90 og.
Att: 23,574
Ref: S Bennett (Kent)