In a land of false prophets, a lamb, supposedly the last of their kind, is brought before four heretic prophets, and is sacrificed before them. Other benefits is the 'Twitch Totem Bar' where viewers can contribute channel points to, resulting in a random reward for the player, and a 'Help or Hinder' event where they can vote on either help or hinder the player's progress. Viewers can customize their follower by entering via a 'Follower Raffle', which will have their username displayed above their character at all times. The game integrates with the streaming website Twitch, via the 'Companion of the Lamb' Twitch extension. Otherwise, the followers can turn against the player, spread dissent, and eventually leave the cult with other followers to prevent this, the player can provide for them, give them gifts, reeducate them, or detain them in a pillory until they stop dissenting. The player must ensure their followers' needs are met by performing sermons and rituals to reinforce their faith, cooking food for them to survive, providing them with shelter, and ensuring the village is clean and sanitary. Followers can be assigned tasks at the base such as gathering resources, building structures, worshipping, performing rituals, sending them to assist the player in battle, or sacrificing them, which can affect the player's abilities and the cult itself. The player can manage their followers at their cult's village. These animals have appearances that can be changed and both positive and negative traits, which can affect how they act in the cult or how they react to the player's actions regarding the cult. The world, which is randomly generated and contains roguelike elements, contains resources to gather, perks and weapons to collect, enemies in the form of rival cultists and non-believers to fight, and other animals to rescue these animals can be indoctrinated into the player's cult. The player must launch roguelike-style crusades and venture out into the game's five regions to defeat enemies and grow their following. Cult of the Lamb is centred around a possessed lamb that is tasked with forming a cult to appease the ominous deity who saved the player character's life.

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