As Spyro searches for the tree, he also searches for another dragon, the Chronicler, who asks Spyro in the same vision to find him. At the same time, Ignitus looks for help against the Apes. After Spyro repels the attack, Ignitus, the leader of the dragons and master of fire, sends Spyro to seek out a tree that Spyro saw in a vision (in the dreams to follow, he gets his powers back, as he lost them at the end in A New Beginning).

Soon after she is gone, the Temple is attacked by the apes. She runs off, leaving Sparx and Spyro alone. Cynder says she's sorry for what she had done in the previous game and wishes to find out where she belongs in the world, currently believing that she does not belong at the temple. Spyro catches up with her and asks her not to leave. The story continues with Spyro following Cynder through the swamp surrounding the Dragon Temple. The Eternal Night continues the storyline established by A New Beginning, which ended with the defeat of Cynder, a black dragon in servitude for an enemy called the 'Dark Master.' In The Eternal Night, a new antagonist - 'Gaul' the Ape King - has risen to power and intends to resurrect the Dark Master on The Night of Eternal Darkness.

Each quill collected gives the player 5 pieces of concept art. Throughout the levels there are forty quills. He can also use this ability to defeat enemies more easily. He can use this ability to jump on platforms which are too fast to land on with his normal speed. This skill allows Spyro to slow down time. Spyro is able to learn the skill of 'dragon time' from the Chronicler. Spyro is required to obtain a certain amount of purple gems to be able to use these skills. Spyro can also use furies, which are big blasts of elemental magic.

They come in different elements fire, ice, electricity and earth. The breaths are tools for defeating enemies. Spyro will learn different breaths from the Chronicler, who is met in Dreams which occur to Spyro during the course of the game.

However, there is a much larger emphasis on exploration and puzzle-solving. Spyro must travel to the end of a level in a linear fashion and defeat the boss at the end of each level, defeating enemies with his combat moves. The gameplay is similar to its predecessor.

Spyro ds eternal night