Reuben Hazell's mistake gave Clive Platt an easy chance to score and the Latics could find no way back against dogged and determined Colchester.
Oldham have taken just one point from their last three games at Boundary Park, with a lack of cutting edge continuing to be their downfall.
Colchester had chances to increase their lead, especially in a one-sided first half, and Oldham boss John Sheridan blasted his team as "shocking" after they were booed off at the end.
For Colchester, this was the eighth away win of a season which has improved dramatically since Paul Lambert took over as manager.
Chris Coyne was outstanding in defence, while widemen David Perkins and Simon Hackney were a regular source of danger.
The U's were gifted and their winner after less than two minutes when Hazell attempted to head back to keeper Greg Fleming.
He could only pick out Platt, who turned ten yards out and hooked his shot beyond the stranded keeper.
Oldham remained all at sea, with Colchester's Perkins granted too much space before he shot straight at Fleming.
The visitors went even closer to doubling their lead on 24 minutes as Hazell needed two attempts to clear Hackney's flighted cross off the line.
Hackney was next to threaten when he seized on a Perkins' throughball but fired wastefully off target from close range.
Steven Gillespie hit the outside of the post ten minutes before the break and Oldham could count themselves lucky to still be in the hunt.
They sprung to life after 47 minutes as Andy Liddell picked out on-loan striker Steve Kabba, whose snapshot was parried to safety by Mark Cousins.
The visiting keeper was much busier after half-time but, on the only occasion Oldham got past him, Deane Smalley's driven effort came back off the woodwork.