The World Eater was designed to prove that not all games need to be massive, with long lists of keywords and complex card interactions and phases. While Onemus has cards exceeding the 700 count, The World Eater is streamlined at a little over 100 cards. It intends to function as a standalone set without booster packs but with possible expansions.

The general goal of a standard run of The World Eater is to defeat the title character, which is a monstrosity spawned from the entropic forces of a black hole. The World Eater is little more than a giant mouth and digestive tract, and seeks to live up to its name by eating as many worlds as possible. Of course, succeeding in its intention would mean the end of all life, human and otherwise, and a group of six sentient beings banded together to form the Astral Guard. Knowing the World Eater is extremely powerful, but also knowing that powerful artifacts exist about the galaxy, the Astral Guard hope to use these artifacts to defeat the World Eater. Players participate as part of the Astral Guard, travelling through planets in hopes of gathering the artifacts they need and fighting against a sole player, the Mastermind.

The World Eater subscribes to the existence of the Dungeon Master (often "DM") popularized by the game Dungeons and Dragons. The DM in The World Eater is called the mastermind ("MM"). He is able to summon NPCs, including the World Eater. In essence, the protagonists are fighting against the mastermind. From this setup comes the victory conditions: the mastermind wins if he is able to summon the World Eater and the Astral Guard wins if they kill the mastermind before he summons the World Eater.