In Cult of the Lamb, the player takes on the role of the leader, a lamb saved from execution by an imprisoned deity known as "The One Who Waits." This deity grants the lamb powers to start a cult in its name, making the lamb both the protagonist and the cult leader.

The main objective of the lamb is to build a loyal cult of followers while defeating four powerful rival deities known as the Bishops of the Old Faith, who are responsible for imprisoning "The One Who Waits."