The Blues' first league trip to Layer Road for 50 years ended in a disappointing 1-0 defeat live on Sky TV. Karl Duguid struck after nine minutes to put the home side ahead, but Town will feel hard done by after referee Lee Probert inexplicably disallowed Jon Macken's second half ‘equaliser'.
Midfielders Sylvain Legwinki and Simon Walton returned to the side with Matt Richards and Gavin Williams dropping out, the Welshman, set for a groin operation this week, failing to make the 16. Richard Naylor kept his place alongside Jason De Vos with Alex Bruce on the bench.
Sylvain Legwinski hit the first serious shot of the game in the seventh minute, his strike from Alan Lee's knockdown flying wide of one-time Town loanee Aidan Davison's post.
Two minutes later the U's went ahead. Former Canary Jamie Cureton was given time to hit a low shot from the edge of the area which the unsighted Lewis Price could only push away. Colchester midfielder Karl Duguid reacted quicker than Darren Currie and squeezed the rebound between Price and the post.
The home side had started very much the stronger and deserved their lead on the balance of the early play. Town had failed to get going with the home side giving the Blues' midfielders little time on the ball.
On 12 a freekick was played to Kevin Watson on the edge of the area but his strike was too close to Lewis Price. In the 18th minute keeper Davison saved Jason De Vos's near post header from Darren Currie's corner.
Colchester were close to increasing their lead on 25 when Simon Walton dallied before playing the ball to Cureton who shot only just wide of Price's goal when he should have scored.
On the half hour, the U's had another gilt-edged chance, Kemal Izzet nodding the ball down to Cureton who shot across the face of goal. Two minutes later, Wayne Brown's 25-yard freekick gave Price little trouble.
Town finally started to show something of their recent form and Macken crossed towards Mark Noble but the loanee from West Ham couldn't control his strike and Davison claimed.
Currie sent a dangerous ball across the Colchester box from the right, then the Blues weren't far away from an equaliser as the former Brighton man found Alan Lee at the far post with a low cross, but the Irish international sent the ball back across the face of goal.
A goal would probably have flattered the Blues who had failed to get going. They had allowed Colchester three excellent chances and were fortunate only to go in one goal down at the break.
Despite the poor showing, Jim Magilton decided against any substitutions. Even without changes, the Blues came out looking a brighter proposition in early stages of the second half. There appeared to be a quicker tempo about Town and Macken saw a shot saved inside the first minute. Sylvain Legwinski was yellow-carded for a foul on Kemal Izzet on 48.
Town thought they were back on terms a minute later when Alan Lee found himself space to shoot inside the area. Aidan Davison saved his strike but Macken was following up to bundle the ball over the line. The loanee started celebrating his first goal for the Blues in front of the Town supporters only to discover that referee Lee Probert had awarded a freekick to Colchester for no immediately discernible reason.
Within a minute, Price made a fine save to block in front of Chris Iwelumo from Karl Duguid's left-wing cross, although Town felt that Sito had been pulled back by the Colchester goalscorer earlier in the move.
On 51 Macken, clearly still unimpressed at the decision to disallow the goal, picked up a yellow card for a foul on Izzet. The loanee from Crystal Palace made way for Billy Clarke in the 63rd minute, the Blues having lost their impetus as the half wore on.
Colchester felt they should have had a penalty in the 68th minute when the ball appeared to strike Richard Naylor on the arm. Fortunately for the Blues Mr Probert decided the ball had hit him on the chest and waved away the appeals.
Clarke came close to an equaliser in the 70th minute when latching on to Lee's knockdown from Legwinski's cross but Davison was out to block the young Irishman's shot.
On 73 Currie's corner struck Clarke but flew wide, then Cureton was booked for timewasting, an increasingly popular pastime amongst his team-mates as the game wore on.
Legwinski volleyed wide, then Lee shot wide as the Blues went into the last 10 minutes still chasing the equaliser. At the other end, Price saved Iwelumo's header.
With five minutes remaining, Dean Bowditch took over from Simon Walton, who had put in the least impressive performance of his time with the Blues. As Town continued to press, former Town defender Wayne Brown was booked for a foul on Lee.
But the equaliser wasn't to come and the home supporters celebrated their first league victory over Town in 54 years at the final whistle.
Colchester had certainly been much the better side in the first half, but the Blues had come back at them after the break and probably deserved the equaliser they appeared to have scored, despite rarely being at their best.
There were too many under par displays all over the pitch, but particularly in midfield where Walton, Noble and Legwinski were less dominant than in previous games, Williams was sorely missed, and Currie was more the frustrating figure of last season than the more effective player of recent games.
Price may well have done better with the goal, although he saw it late, and up front Lee and Macken were unfortunate not to have been awarded an equaliser which may well have given the Town the momentum to go on to win the game.
But Jim Magilton's men never reached the heights of their recent performances and will need to improve to get back to winning ways against West Brom in a fortnight.
Town: Price, Sito, Harding, Naylor, De Vos, Walton (Bowditch 85), Legwinski, Noble, Currie, Lee, Macken (Clarke 63). Unused: Supple, Richards, Bruce. Att: 6,065.