Hugo Rodallega scored the winner at White Hart Lane 10 minutes from full-time after Carlo Cudicini allowed the winger's tame shot to squirm past him in what was the goalkeeper's first start since his horrific motorcycle accident.
It was a remarkable result for a Latics side who had conceded 10 goals in their opening two Premier League games and nine in the corresponding fixture last season.
It also cast doubt on Spurs boss Harry Redknapp's claim he has a squad capable of competing both domestically and in the Champions League.
Indeed, Redknapp's fears about complacency following last season's goal glut against the Latics and Wednesday night's historic European victory against Young Boys appeared to have been realised.
Spurs made a sluggish start and Rodallega flashed an early warning shot wide before poor defending from an eighth-minute corner saw Steve Gohouri smash the ball against the crossbar from Mauro Boselli's knockdown.
Tottenham were conceding possession in dangerous areas, while a clumsy defensive clearance nearly ricocheted past Cudicini.
The home side eventually got going and Jermain Defoe was given the freedom of the Wigan penalty box to fire a low shot which brought the best out of Ali Al Habsi, the on-loan Bolton keeper starting ahead of Chris Kirkland, who was not in the squad.
On the half hour mark, Michael Dawson became the first player booked for cutting down Mohamed Diame 25 yards from goal.
The visitors were demonstrating the kind of defensive nous sadly lacking in their opening two Premier League thrashings, with Peter Crouch effectively shackled by Gohouri and Antolin Alcaraz.
Crouch did clip a ball through to Defoe five minutes before the break, which the latter poked narrowly wide with the outside of his right foot.
Hendry Thomas joined Dawson in the book after felling Aaron Lennon shortly before a disappointing half drew to a close.
Spurs made a double-substitution at half-time, bringing on Roman Pavyluchenko and Niko Kranjcar for Crouch and Benoit Assou-Ekotto.
Despite a comfortable first half, Wigan would have been wary it was only 1-0 at the same stage of the corresponding fixture last season.
However, although Pavyluchenko mistimed a header from Lennon's cross, the Latics' blanket defence was holding firm.
Spurs began to throw both Ledley King and Dawson forward as a breakthrough began to look less and less likely.
The visitors replaced lone front man Boselli with Jordi Gomez midway through the half, while Spurs soon followed suit by bringing on Giovani Dos Santos for Lennon.
Kranjcar saw yellow for sending Thomas tumbling 16 minutes from time, before he himself got Maynor Figueroa cautioned.
Having spent almost the entire half penned in, Wigan suddenly went on the attack.
Alcaraz somehow missed the target from point-blank range after the assistant referee wrongly kept his flag down and Gomez also volleyed over the top.
Both chances came from crosses by Rodallega, who found the net himself 10 minutes from time after Cudicini fumbled his weak shot into the net.
Tottenham poured forward in search of an equaliser and Tom Huddlestone volleyed just wide, Defoe found the side-netting and Kranjcar and Dawson both forced acrobatic saves from Al Habsi.
Wigan brought on James McArthur for Ronnie Stam in the closing moments, while Spurs screams for handball against Alcaraz were ignored by referee Phil Dowd.
Younes Kaboul wasted a glorious chance to equalise in stoppage-time when he glanced Kranjcar's free-kick wide.