An exploration-driven 3D metroidvania/first-person shooter hybrid and sequel to Metroid Prime (2002) in which Samus lands on Aether, an intricate planet torn into light and dark versions of itself, to help its remaining inhabitants defend against the invaders from its dark incarnation by traversing both the light and dark worlds, acquiring new power-ups and braving oppressive environments.

The bounty hunter Samus Aran is dispatched to the planet Aether after the Galactic Federation loses contact with a squad of Marines stationed there. She arrives to find the troops slaughtered and soon learns of a devastating conflict: decades earlier, a meteor split Aether into two mirrored dimensions, spawning a malevolent shapeshifting race called the Ing who wage war on the peaceful, near-extinct Luminoth. Enlisted by the last Luminoth sentinel to recover the planet's stolen light energy, Samus must journey between the world of light and its poisonous dark counterpart, battling the Ing, Space Pirates, and a mysterious doppelganger known as Dark Samus.