In the final chapter of the trilogy, players find Sypro teaming up with an unlikely ally - Cynder, his former enemy, to face his most challenging mission to date. As the Dark Master's evil envelopes the world like a plague, Spyro must fulfill his destiny and unlock the true power of the purple dragon within him to stop the Dark Master in his tracks.

The game introduces two never before seen elements into the Spyro universe: Spyro can now fly at any time and players can drop-in/drop-out with the new cooperative feature. The co-op feature allows players to have the option of completing the game as either Spyro or Cynder, giving them more freedom to explore Spyro's world in completely new ways.