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".

The teens of Berk find a mysterious girl named Heather on Thor's Beach. While Hiccup and the other teens openly welcome the newcomer, Astrid's jealousy turns to suspicion when she notices Heather is taking an unusual interest in the Book of Dragons.

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.

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.

During Berk's annual Bork week celebrations, Hiccup is granted access to Bork the Bold's private and personal archives. When he finds information and a map about an island inhabited by Night Furies within Bork's notes, Hiccup is determined to bring Toothless to his family.

Mildew has betrayed the Vikings of Berk and allowed Alvin the Treacherous to kidnap Hiccup and Toothless. Astrid and Stoick must rescue them from Outcast Island along with help from a new friend.

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.

A Terrible Terror training competition leads to a heated rivalry between Fishlegs and Snotlout, allowing Alvin to kidnap Meatlug. The kids must use their newly trained Terrors to rescue their friend.

When the dragon riders discover a frozen Skrill, a lightning-powered dragon revered by the Berserkers, they scramble to get it off Berk.

Tuffnut goes undercover to help the riders rescue a Skrill.

Snotlout is expelled from the academy; Alvin returns to Berk to make amends.

Alvin reveals he trained the Screaming Death to attack Berk and destroy the island's inhabitants and only Snotlout and Hookfang can save Berk before it's too late. Meanwhile Hiccup gets ready for a final fight against Dagur to save Toothless and end the barbarians invasion of Berk once and for all.