The midfielder, 22, rejected the offer of a new deal from Killie manager Lee Clark, instead opting to move south on a two-year contract despite interest from Aberdeen.
Kilmarnock will receive compensation for the player which could be as much as £180,000. St Mirren will also receive a solidarity payment for their part in Slater’s development.
He will link up with fellow Scot Denny Johnstone at Colchester who scored 14 goals while on loan at Morton last season.
Slater leaves Kilmarnock after 85 appearances over three seasons. He made his debut in a 2-2 draw against Motherwell in December 2012.