Hiccup had discovered Mildew framed the dragons but has destroyed all evidence of it, therefore he must prove of their innocence in order to get them back. Meanwhile, Alvin the Treacherous of the Outcast Tribe are on the mission to raid the Isle of Berk in order to find and capture the "Dragon Conqueror".
Heather's betrayal to Berk caused the Book of Dragons to fall into Alvin the Treacherous' hands, and Heather's imprisonment on Berk. In order to get the book back from Alvin, Astrid disguises herself as Heather and goes into Outcast Territory. Towards the end of her mission, Astrid learns and confirms Heather's true motives for helping the Outcasts.
Berk's annual festive sporting competition, the Thawfest games, is underway and all the teens are participating with the dragons for the first time in Viking history. Hiccup is determined to finally best Snotlout, who constantly gloats about being the reigning Thawfest champion, but Hiccup's successes begin to make him arrogant and boastful, much to Astrid's displeasure and disappointment.
Sudden lightning storms are endangering the residents of Berk and it is believed Thor is angry at the island. Mildew leads the superstitious villagers into blaming Toothless, "the unholy offspring of lightning and death itself", for the lightning, leaving Hiccup to find the true answers for Thor's sudden destructive anger.
A rogue dragon: a Whispering Death, shows up in Berk, tearing up the village. He's on a mission to find Toothless and settle a score. Despite Hiccup's efforts to help, Toothless insists on facing the dragon alone. But unlike their past battle, Toothless's inability to fly may prove to be his undoing.
Dagur the Deranged visits Berk to renew a peace treaty between the Berserkers and Berk, and the dragons are put into hiding to dispel rumours that Berk is training a dragon army. But when Ruffnut and Tuffnut begin to fight, their dragon, Barf and Belch, is left out of control. The Viking youths must bring the twins back together to control their dragon and avoid provoking Dagur to war.
Caught in a waterspout, Toothless' prosthetic tail is damaged, rendering him unable to fly and thus leaving him, Hiccup and Snotlout stranded on Outcast Island. The three must work together to repair the damage, overcome the rivalry between Hiccup and Snotlout and return home to Berk before they are captured by Alvin and the Outcasts.
Certain that Alvin is planning an attack on Berk, Stoick institutes flight restrictions on the dragon academy. Hiccup, certain that Alvin will be using his newfound dragon-training knowledge to bolster his attack, forms a secret “Dragon Flight Club” in order to train the kids to defend Berk against Alvin’s dragon army.