Spyro must save the Dragon Realms from the Evil Red Dragon who has planted light-sapping Dark Gems all over the Dragon Realms in an attempt to capture and control the world. With the help of his allies, Spyro must seek out and destroy all of the Dark Gems to return the lands back to normal and to save the Dragon Realms from the evil dragon's tyrannical control.

The fierce purple dragon will travel across dark, mysterious lands in which the environments shift from evil to good in real-time - affecting enemies, music, lighting, objects, sky and more. Outfitted with mighty new abilities including the Wall Kick, Tail Swing and Ledge Grab, Spyro will fight his enemies with powered-up breath attacks - burning opponents with Flame Breath, deep-freezing rivals with Freeze Breath, obstructing adversaries with Water Breath and destroying mechanical enemies with Electric Breath. In addition to playing as the heroic leader Spyro, gamers will also have the opportunity to play as weapons master Hunter the Cheetah, dive-bombing penguin Sgt. Byrd, loyal sidekick Sparx the Dragonfly or the all-new weapons-equipped, climbing Blink the Mole.