The sending-off of striker Lee Hughes in the final minute was the only cloud on Oldham's horizon as they ground out a deserved victory at Sixfields.
It was Northampton's first home defeat in the League since Good Friday and manager Stuart Gray admitted he was disappointed with his players' inability to keep the ball.
He had no qualms with the decisive penalty award by referee Paul Taylor, given after Hughes tumbled in the box under a challenge from three Northampton players which allowed Andy Liddell to stroke home the resulting spot-kick.
Hughes had struck the post in the final minute of the first half and it was always the visitors who carved out the better chances as the same player tested Frank Fielding in the home goal with a low drive in the 12th minute.
Darren Byfield, signed on-loan from Doncaster on Friday, could have scored after 59 minutes when he met a near post cross from Hughes with a snapshot, only to see Fielding push the ball around the post for a corner.
Byfield missed the target with a decent opening with 20 minutes left but Northampton chances were even thinner on the ground - Latics goalkeeper Mark Crossley only once being required to save a shot in the entire game.
Northampton could take heart from the performance of debutant Kyle Walker who was signed as defensive cover from Sheffield United in midweek and he made some promising forays down the right.
For the visitors, the pace of leading scorer Chris Taylor was only let down by some inaccurate shooting while former Northampton loan player Daniel Jones also acquitted himself well against his former club.
Both sides face FA Cup replays this week with Northampton first up on Monday when Leeds United are the visitors at Sixfields.