(Please note, the story jumps between characters perspectives. For the sake of convenience, a character's full "scene" in a chapter may be condensed together for the sake of cohesion.)
The story opens with Spyro and Cynder awakening a bit after defeating Malefor at the end of Dawn of the Dragon. Both are left exhausted and tired from their previous battle and Spyro is near powerless at the moment because of that. The two try to recover and explore around, flying through the Valley of Avalar as seen at the end of Dawn of the Dragons. They explore a bit before stopping to rest but are ambushed by a group of apes, who somehow are still alive despite Malefor cursing them for being skeletons previously. They capture Cynder, subdue Spyro, and toss him into the river.
Despite being tossed, he somehow awakens at the dragon temple the Guardians are at, which is now suspended in the sky do the the world's upheava from the conflict with Malefor. The Guardians fished Spyro out of the river that morning. He tells the Guardians what happened and they agree to look for Cynder
Meanwhile, a teenager named Zach gets off school for the summer. Zach had been a fan of the Legend of Spyro for a while and nearly considered them to be family in a sense. He has been having strange dreams about the dragon realms, as well as seeing things like Spyro and Cynder's battle with Malefor as well as Cynder and Spyro confessing their love for one another in his dreams. Though he intends to have an easy summer, he somehow ends up being transported into the dragon realms, seemingly falling through the sky and landing by a river (Silver River) in the wilderness. He is also turned into a dragon. Eventually, he is found by a dragonfly named Ray who, under the impression he is trying to get to Warfang most likely, tries to guide him 'home'. Ray eventually guides him through a dragonfly village, where Ray's father breaks up a mob who were over curious about a dragon walking through their village, and then onward to the "Cliffs of Despair", named for a few days ago when a group of dragonflies went missing while trying to make a home there.
Ray parts with Zach near the cliffs, leaving him instructions to follow the cliffs home. Zach enters a few caves in the cliffs. Here, Zach encounters an ape who tries to capture him. Zach flies into another cave but finds a group of apes who are on patrol and are searching for him, but he instinctually activates an invisibility power of his. He manages to hide from the apes and eavesdrop on them, hearing them talk about Cynder and their plans. Zach goes to investigate and manages to sneak into their stronghold where he finds Cynder held prisoner.
Cynder had previously been visited by an ape who had trapped her with the same green magic chain Malefor used on her before and told her they had some kind of plans for her. He offers her her old place as a general in the Dark Army but she declines. The apes state some new master of his has plans with her, implying they will attempt to mind control her into being the Terror of the Skies again. Cynder is under the impression Spyro died after being tossed into the river and is devasted.Zach talks to Cynder a bit, and after an introduction, he is informed of the circumstances surrounding the chain and how only on as strong as Malefor could break it. Zach suggests Spyro but Cynder thinks he is dead to to which Zach confinds in her that Spyro is likely still alive and it is unlikely he died to an ape that easily. Zach accidentally attracts an ape guard into the room. The guard smacks Cynder in anger for waking him up with her talking and draws blood (Zach was invisible at this time) and leaves. Though irritated at Zach for attracting attention, Zach accidentally activates other powers he has and heals Cynder, causing her to thank him.
Cynder finds he is unable to free her, so he is instructed to go get Spyro for help. She tells Zach about the flying temple and how to get there. Zach flees out of the room and into the ape fortress but accidentally triggers their defenses by getting spotted. He is chased through the corridors of the cave-like structures and repeatedly tries to hide from his pursuers. After evading the apes, he finds his way back through the chambers he entered through and exits through the waterfall-hidden entrance he used before after being cornered there by apes. Zach nearly drowns however and is knocked out for a bit. The apes think he did not survive the fall. Zach after what seems to be a night, wakes up near a forest age, pulls himself together, and goes wandering off to find the temple.
While this had happened, an ape beat Cynder after she attempted to attack him when entering her room and was apparently brought to be experimented on.
Meanwhile, with Zach, he dodges ape patrols in the forest, finds a spirit crystal for the first time which reinvigorates his energy, and continues on, eventually spotting the floating temple as Cynder had instructed him.
Spyro while all this had happened, had a dark dream where Cynder chastised him for leaving her alone and letting her get captured as she did. He is plagued by these intrusive thoughts, born out of worry. He wakes up and is comforted by Terador, who said he sadly could not find Cynder. Spyro insists he go to find her, but Terrador tells him he is too weak to do so and that others are trying their best to find her. He tells Spyro that, despite saving the world, he does not have to do everything and that he should simply rest until he is better, then he can go find her. He reminds Sypro that they do not know where she is yet. Spyro feels dejected and useless that he could not find Cynder.
Once Zach arrives, however, he calls down to the temple and is briefly mistaken for an intruder before he explains who he is and that he knows where Cyndeer is. He informs Pyor and Terrador, but is reluctant to help himself since he doubts his abilities in combat but Spyro insists on his help. Zach eventually agrees to accompany S Pyro back to save Cynder.
