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This article contains plot details.
Three years after the last game, Spyro and Cynder were released by a group of Grublins. The Grublins then chained the two together with an invisible string. This string was generated by two glowing snakes placed around their necks. Under Malefor's orders, they were then taken to the Catacombs in order to be sacrificed to an earth Golem.
When they awoke, they found themselves chained in the Catacombs. Soon after, they were attacked by the Grublins and the Golem. Due to being chained together, the two couldn't fight the Golem. However, Hunter appeared and shot the Golem in the eye, causing it to retreat. It was then revealed that three years ago, Ignitus sent him to find Spyro and Cynder.
The trio narrowly escaped the Catacombs and the Golem's arm was ripped off in the process. Once they made it to the Enchanted Forest, Hunter told them that Malefor had returned and covered the land shadow. He also reclaimed the Dragon Temple and had been waging war ever since. Spyro began to blame himself for letting everyone down but was reassured by Cynder that some things were beyond his control.
Hunter's tribe suddenly captures them as Chief Prowlus didn't trust dragons due to Malefor and Cynder. Spyro and Cynder then saved the tribe's village from Grublins and found a missing villager named Meadow, proving to Prowlus that they weren't evil. The two dragons were then led by Hunter through the Forbidden Passage and to the city of Warfang. Warfang was under attack by an army of Grublins and the Golem.
Spyro and Cynder defeated the army, killing the Golem in the process. They were then reunited with the Dragon Guardians. However, that night Malefor gave Warfang a message. He has awakened the Destroyer, a beast that recreates the world by bringing about its destruction. To due this, it would have to complete a circle around the world called The Ring of Annihilation. This would make a Belt of Fire spread over the world, burning everything in its path.
A plan was created by Ignitus to stop it from underground. Spyro and Cynder opened the doors to the Ruins of Warfang from the inside. This would enable them to reach the Destroyer's destination. Along the way, Spyro was worried about what was going to happen and about ending up like Malefor. He was comforted by Ignitus telling him that Spyro being the only good purple dragon was nature's way of balancing itself.
Reaching their destination, Cynder thought of destroying the Dam, which would flood the valley and halt the Destroyer. The three dragons managed to do so and destroyed the dark crystal that was controlling it. However, Malefor used his magic to take control and had the Destroyer complete its mission.
Ignitus led Spyro and Cynder through the belt of fire while everyone else headed underground. However, Ignitus ended up sacrificing himself to make sure Spyro and Cynder got through. In his grief, Spyro turned into Dark Spyro but Cynder pulled him out of that state by telling him that he wasn't alone. They then made their way through the Burned Lands and the Floating Islands, where they finally confronted Malefor.
Malefor proceeded to taunt Spyro, saying that they had more in common than just their color. Spyro claimed that he was nothing like Malefor and the older dragon freed him and Cynder of their chains. Malefor claimed that his influence over Cynder was still there and that she led Spyro into the Well of Souls in order to free himself. Cynder denied that but then said that she didn't truly know anymore. At this moment, Malefor took control of her again.
Cynder relentlessly attacked Spyro while Malefor told him that there were many purple dragons before him. He proceeded to tell Spyro that their true roles were to resurrect the Destroyer and the Golems of the Deep in order to bring about "The Great Cleansing". Spyro denied this while Cynder kept attacking him and Malefor just laughed manically.
Cynder demanded to know why Spyro refused to fight back and he replied that she left him nothing to fight for. This caused Cynder to break free and she told Spyro that there is always something. Malefor then became enraged and chained the two back together. Saying that Cynder would share Spyro's fate, he attacked them both.
During the battle, the Destroyer completed The Ring of Annihilation, beginning the destruction of the world. They continued to fight and due to a joint attack, Malefor was thrown down to the planet's heart. Malefor claimed that he was eternal and as such, could not be defeated. Just then, the spirits of the Ancients dragged Malefor into the planet's heart, sealing him away.
Once he was gone, Spyro and Cynder were no longer chained together. However, the planet was still breaking apart. Spyro was given hope by Ignitus' spirit and told Cynder to flee. Cynder refused and Spyro unleashed a powerful fury wave. As he did this, Cynder whispered that she loved him. The fury wave reconstructed the world and the survivors resurfaced, gazing at the stars which formed the shape of a dragon.
The Chronicler chose Ignitus to be the next Chronicler of this new age. The old Chronicler told Ignitus that he tried his best but he couldn't find any trace of Spyro in the book of dragons who have died. While Ignitus looks through the book, the Valley of Avalar is shown. Spyro and Cynder were seen flying through the air, finally able to live their lives in peace.
The game received generally mixed reviews.