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Five years after the Viking villagers of Berk and the dragons made peace,[a] Hiccup and his Night Fury, Toothless, map out unexplored lands. His father, Stoick the Vast, wants him to succeed as chieftain, although Hiccup feels unsure if he is ready.
While investigating a burnt forest, Hiccup and Astrid discover the remains of a fort encased in ice and meet a group of dragon trappers. Their leader Eret attempts to capture their dragons for their employer, Drago Bludvist, who plots to capture and enslave all dragons into becoming his soldiers. Hiccup and Astrid escape and warn Stoick about Drago. Stoick fortifies Berk to prepare for battle. Hiccup, however, refuses to believe war is inevitable and flies off to talk to Drago. Stoick tries to stop him, explaining that he once met Drago at a gathering of chieftains, where Drago had offered them protection from dragons if they pledged to serve him; they refused him, so he had his dragons attack them, with Stoick the sole survivor.
Undeterred, Hiccup flies off with Toothless in search of Drago to try to reason with him. They instead meet a mysterious dragon rider, who is revealed to be Hiccup's long-lost mother, Valka, who was assumed to have been killed by a dragon after being carried off during a dragon raid. She explains that, like her son, she could not bring herself to kill dragons, so she's been rescuing dragons from Drago and bringing them to an island nest created out of ice by a gigantic, ice-spewing alpha dragon called a Bewilderbeast, which is able to control smaller dragons by emitting hypnotic sound waves. Stoick and his lieutenant Gobber track Hiccup to the nest, where Stoick discovers his wife is alive. Meanwhile, Astrid and the other riders force Eret to lead them to Drago, who captures them and their dragons and, learning of Berk's dragons, sends his armada to attack the dragon nest. He also attempts to execute Eret, but Astrid's dragon, Stormfly, saves him. A grateful Eret later helps her and the others escape.
At the nest, a battle ensues between the dragon riders, Valka's dragons, and Drago's armada, during which Drago reveals his own Bewilderbeast to challenge the alpha. The two colossal dragons fight, ending with Drago's Bewilderbeast killing its rival, becoming the new alpha, and seizing control of all the dragons. Hiccup tries to persuade Drago to end the violence, but Drago orders his Bewilderbeast to have Toothless kill him. The hypnotized Toothless fires a plasma bolt toward Hiccup, but Stoick pushes him out of the way and is killed instead. The Bewilderbeast momentarily relinquishes control of Toothless, but Hiccup drives Toothless away in a fit of despair and anger over his father's death. Drago maroons Hiccup and the others on the island and rides Toothless, again under the control of the Bewilderbeast, to lead his army to conquer Berk. The group holds a Viking funeral for Stoick, and Hiccup, having lost both his father and dragon, is unsure what to do. Valka encouragingly tells him he alone can unite humans and dragons. Inspired by her words and his father's, Hiccup and his allies return to Berk to stop Drago by riding the baby dragons, which are immune to the Bewilderbeast's control.
Back at Berk, they find that Drago has attacked the village and taken control of its dragons. Hiccup frees Toothless from the Bewilderbeast's control and confronts Drago, but the Bewilderbeast encases them in ice. However, Toothless blasts away the ice and enters a glowing super-powered state, making him immune to the Bewilderbeast's control. Toothless then challenges the Bewilderbeast to protect his rider, repeatedly shooting it in the face, which breaks its control over the other dragons, who side with Toothless as the new alpha. The dragons fire at the Bewilderbeast until Toothless fires a final massive blast, breaking its left tusk. Defeated, the Bewilderbeast retreats with Drago on its back.
The Vikings and dragons celebrate their victory, and Hiccup is made chieftain of Berk, while the dragons from both Berk and Valka's sanctuary accept Toothless as their new alpha. Berk undergoes repairs, with Hiccup feeling confident that they will defend their peace with their dragons.