Darkness Comes Rattling follows the Tribes of Man in their quest to save the world of Tallil from Darkness, a colossal snake that has swallowed the sun. The players must cooperate as they face the challenges of their world, including the formidable shadows that are the minions of Darkness. Eventually, they must choose the bravest among them to enter the mouth of Darkness and rescue the sun.

Each round of the game (known as a "day") is divided into three phases: the Dawn phase, the Challenge phase, and the Dusk phase. In the Dawn phase, each player uses their actions to move about, purify corruption, scout challenges, and share items. In the Challenge phase, each player undertakes a challenge. If they succeed, they gain rewards; if they fail, they incur penalties. In the Dusk phase, game upkeep is performed.

In order to win the game, the players must choose one warrior to enter Darkness as their champion. While the champion battles inside Darkness and attempts to reach the swallowed sun, the other warriors must still defend Tallil from the encroaching shadows, lest they corrupt the world and plunge everything into eternal night. If Darkness finishes swallowing the sun, or the shadows gain too much influence in the world, then the players lose the game.