Gavin Massey forced in the opener and defender Tom Eastman's 71st-minute far post header proved the clincher for the visitors.
After a dreary opening half-hour the game finally came to life when Colchester had penalty appeals rejected after Carlisle defender Sean O'Hanlon slid in to divert Billy Clifford's cross for a corner.
Liam Noble provided Carlisle's principal threat, curling a right-footed shot just over the angle of post and bar from 25 yards before he almost caught out U's goalkeeper Sam Walker with a cross from the left, which looked to be dropping under the crossbar until Walker recovered his balance to push it over for a corner.
The second half continued in similar vein with precious little goalmouth incident until the 65th minute when Colchester grabbed the goal which settled their final-day nerves.
Clifford shook the Carlisle crossbar with a shot from just inside the area and Massey got his head to the rebound to send the ball bobbling in by the right hand post as Carlisle goalkeeper Mark Gillespie scrambled across his line in a despairing attempt to keep it out.
It was not a classic goal, but just what the U's and their 364 travelling fans ordered against a lacklustre Carlisle side, whose League One place was already safe.
Colchester made certain of victory in the 71st minute when David Wright's looping ball from the by-line was headed back across goal and into the net by Eastman.