Spyro starts out following Cynder through the area around the Dragon Temple. When he catches up to her, she tells him that she must leave. Spyro asks her not to go, but an army attacks the Temple while they are talking. As Spyro goes to battle, Cynder runs off. Ignitus, the leader of the Dragons, sends Spyro on a journey to find the tree he has been seeing in visions. On his quest, Spyro is captured by pirates and forced to participate in gladiatorial combat. As he escapes the pirates, Spyro learns that the Ape army is at the Mountain of Malefor, trying to revive the Malefor using the lunar alignment known as the Night of Eternal Darkness. They are also holding Cynder prisoner.
Spyro finds a dragon known as the Chronicler, who tells him that Malefor was the first purple dragon. The growth of the dragon's abilities allowed Malefor to learn almost every elemental power. The Elder dragons exiled and sealed him away, but not before he taught the Apes to use magic. The Chronicler tells Spyro that he must hide from the Apes until he is stronger.
But Spyro must save Cynder. When he reaches the mountain, Spyro battles the Ape King, Gaul. As they battle, the lunar alignment starts and Spyro absorbs the power to kill Gaul. As the alignment passes, the mountain crumbles. Spyro uses his power to encase Cynder, Sparx and himself in crystal to protect them.
The story continues in The Legend of Spyro: Dawn of the Dragon.
Much like Spyro: New Beginnings, Spyro must travel to the end of every level and defeat a boss, but not before defeating a large range of enemies. The player will travel around different areas of The Dragon World learning different breath types, ice, electric, earth. In combat, when Spyro collects enough purple gems Spyro can unleash a powerful elemental attack which is called “Fury Attacks” which can destroy most enemies, but does not damage bosses. Spyro can also use a new ability called “Dragon Time” which lets the player slow downtime for a certain amount of time which helps the player jump platforms that are too fast for him in normal time and he can also use it to defeat enemies. The player can also collect “Quills” that let the player unlock concept art.
- Elijah Wood as Spyro
- Mae Whitman as Cynder
- Billy West as Sparx
- Gary Oldman as Ignitus
- Martin Jarvis as The Chronicler
- Kevin Michael Richardson as Gaul, Terrador, Sniff
- Corey Burton as Volteer, Additional characters
- Jeff Bennett as Cyril, Mole-Yair, Scratch, Additional characters