It has been five years since Laura and Carmilla vanquished the apocalypse and Carmilla became a bona fide mortal human. They have settled in to a cozy apartment in downtown Toronto; Laura continues to hone her journalism skills while Carmilla adjusts to a non-vampire lifestyle.

Their domestic bliss is suddenly ruptured when Carmilla begins to show signs of "re-vamping" - from a fondness for bloody treats to accidental biting - while Laura has started having bizarre, ghostly dreams. The couple must now enlist their old friends from Silas University to uncover the unknown supernatural threat and save humanity - including Carmilla's.