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In a fitting reflection of the relationship shared with Amaterasu, the powerful sun goddess who embodied a wolf in Ōkami, the child deity Chibiterasu manifests in the form of a white wolf cub in Ōkamiden. The game is set nine months after the events of the previous game, and the young sun god is summoned to battle a sinister force that has drained the landscape of colour, leaving it withered and faded where once it was luminous with life.

Ōkamiden shares many gameplay elements with its predecessor, including the paintbrush used as a weapon against enemies and for puzzle solving. Chibiterasu can also team up with various companions during the game for additional abilities.