The 20-year-old spent the second half of last season on loan at National League side Rochdale, making 25 appearances and scoring a penalty in the shootout that saw the club secure promotion to League Two via the play-off final at Wembley.
Perry's move to newly-promoted Cambridge comes shortly after he committed his long-term future to Coventry by signing a new contract with the Premier League club last month. He now links up with his new team-mates ahead of their pre-season training camp in Spain.
The defender expressed his delight at finally getting the move over the line.
"I'm buzzing," Perry said. "It has been a long time coming but I am delighted to finally be here. I had a call with the gaffer and everything he said seemed to fit me and where I am at in my career.
"I just want to get better and help the team and I think this is the perfect place to do that."
Cambridge boss Neil Harris was equally pleased to bring in the young defender.
"We are delighted to welcome Callum Perry to the football club," Harris said. "He had a fantastic year last season and offers great balance to our team.
"His left-footed ability and versatility strengthen our backline, allowing him to play a number of positions across the defensive unit. We look forward to helping Callum develop and progress as a young player on his journey to the top."
Perry has represented Coventry City at both Under-18 and Under-21 level, captaining the latter side, and has also been an unused substitute for Frank Lampard's senior squad. The move to Cambridge represents a significant step up for the defender, who will now test himself two divisions higher than his previous loan spell after helping fire Rochdale back into the Football League.
Cambridge, who finished third in League Two last season to secure automatic promotion, have made Perry their latest addition of a busy summer of incomings.
The left-footed centre-back's ability to operate across multiple positions in defence gives Harris additional flexibility as he shapes his squad ahead of life in the third tier, with the club keen to build on last season's promotion-winning campaign rather than simply consolidate.