| Spoiler warning!|
This article contains plot details.
The story begins several weeks after A New Beginning. Spyro has been following Cynder around the swamps and jungle of the Dragon Temple, having heard from Sparx that she had been sneaking out. After having caught up to her, Cynder told Spyro that she was leaving the Temple because she felt guilty about what she did while under Malefor's control and that her destiny is somewhere out in the world. Cynder then leaves, despite Spyro's pleas. Before he could chase her, he collapsed and was pulled into a dream. A voice in his dream spoke and Spyro regained his fire ability. He then saw a vision of a great tree and the voice was revealed to belong to a dragon called the Chronicler.
After Spyro woke up, the Dragon Temple came under attack by an ape army. Spyro defeated them and Ignitus tried to locate Cynder. Instead, he saw a vision of Spyro at a great tree. Then, Spyro claimed that he kept having haunting visions of a mountain. In his visions, this mountain was covered in darkness beneath two moons. Terrador realized that the mountain Spyro was seeing was the Mountain of Malefor.
Spyro then reveals that the Chronicler came to him in his dreams and showed him that tree. This shocked the Guardians and Ignitus explained that the Chronicler was an ancient dragon who had immeasurable wisdom and was often interwoven with tales of doom. They became increasingly worried about an eclipse due to the Celestial Moons and that they were no longer safe at the Temple. Volteer and Cyril were sent to the mainlands to learn of any news, Terrador was sent to the Shattered Vale in order to warn everyone, Ignitus stayed behind to search for Cynder, and Spyro was sent to the Ancient Grove in order to find the tree from his dreams.
During his search, Spyro was once again summoned by the Chronicler. This time, he regained his ice abilities and was shown a vision of an ape king leading an army to the Mountain of Malefor while screaming, "...The Well of Souls!". The Well of Souls turned out to be another name for the mountain. When Spyro finally woke up, he found the tree. However, it turned out to be a monster called Arborick.
After defeating Arborick, a group of Skavengers appeared. The leader of the Skavengers, Skabb, wanted Arborick for entertainment in a fighting arena. They also wanted Spyro to "cooperate" and knocked him unconscious. When Spyro awoke, he found himself in a cell aboard a ship called the Fellmuth Arena.
Spyro won battle after battle in the arena. Shortly after defeating the Blundertails, Spyro was summoned by the Chronicler and regained his earth powers. The Chronicler told him more about the Well of Souls and the Night of Eternal Darkness. He then told Spyro that he could be found in the Celestial Caves of the White Isle. Afterwards, Spyro received a message from a fellow prisoner called Hunter of Avalar. The message told Spyro that Hunter was now his ally.
In a final match aboard the ship, Spyro was forced to fight Cynder. She told him her escape plan but it didn't go as planned when an ape army attacked the ship and captured her. During the chaos, Spyro defeated Skabb and escaped. Afterward, the Chronicler once again summoned Spyro. In this dream, Spyro regained his electric abilities and saw a vision of Cynder in chains. She was brought before Gual, the ape king.
After arriving at the White Isle, Spyro overcame challenges that tested his elemental skills. Finding the Chronicler, he told Spyro about Gaul. Gaul was the one who led the raid of the Dragon Temple on the night of Spyro's birth and who stole Cynder's egg. Spyro asked to know about Cynder's past and what would happen to her. Learning that Cynder would return to Malefor's side upon his return, Spyro refused to believe it.
The Chronicler then told Spyro about Malefor. Malefor was the first purple dragon and his power allowed him to master every elemental power. He was later exiled by the Dragon Elders and built an army of apes. Malefor's malice split the earth, in turn creating the Well of Souls. It was there that the apes established an effort to revive Malefor during the Night of Eternal Darkness. Spyro then insisted on helping Cynder, even though the Chronicler wanted him to hide from the apes until a later time.
Later, Spyro arrived at the mountain and confronted Gaul in the Well of Souls. After being zapped with Gaul's staff, Spyro was rendered weak and drained of his powers. Cynder was then ordered to attack Spyro but she attacked Gaul instead. As a result, he knocked Cynder out and challenged Spyro himself. During the fight, the lunar eclipse occurred. The evil energy created by it was channeled through Spyro, transforming him into Dark Spyro. Under Malefor's influence, Dark Spyro turned Gaul into stone before killing him.
Dark Spyro then leaped back into the beam of evil energy. However, he was knocked out of it by Cynder when she awoke. Spyro apologized but Cynder forgave him. The battle with Gaul caused the mountain to start collapsing. Cynder spotted an opening that Spyro, Sparx, and herself could escape through.
However, Spyro was weakened from his battle and told the two to leave without him. They refused and the opening soon collapsed. Having recalled the Chronicler's words, Spyro used Time Fury to freeze Cynder, Sparx, and himself inside a crystal. This crystal protected them from harm as the mountain continued to collapse.
Later, the crystal was seen among the ruins. The Chronicler spoke to Spyro telepathically. He said that when Spyro awoke, the world as he knew it would be different. However, he would not be alone and he would have allies.
The game received mixed to positive reviews.