The 22-year-old, who has signed a one-year contract, joins defender Craig Barr and striker Mark Stewart at the Scottish Championship club.
Johnston came through Kilmarnock's youth ranks to make the Premiership side's first team.
But he moved to Kirkcaldy last summer and played 34 times.
Barr, 30, had been at Stark's Park for three seasons after leaving Airdrieonians and played 17 times as Rovers dropped to League One.
The 29-year-old Stewart joined Rovers at the same time, from Derry City, and scored five times in 36 appearances last season.
Former Kilmarnock winger Chris Johnston has become the third player to sign for Dumbarton this summer after leaving relegated Raith Rovers.