Every decade, Aurvandil's Fire arrives to Berk, inviting a ghostly dragon, the Flightmare, to the village. Astrid, with the help of Hiccup and Fishlegs, is determined to defeat this dragon, which seemingly "froze" her uncle with fear, in order to restore her family name. Meanwhile, Ruffnut and Tuffnut create a bunker at the Academy to hide from the Flightmare, allowing everyone in except Snotlout, instead demanding a superfluous amount of unusual tasks, such as bringing rainbow chickens, singing Terrible Terrors, and fish dressed like Stoick to mess around with him.

When the nearby islands begin to disappear and the dragons that used to inhabit them begin migrating to Dragon Island, the teens discover that the cause of this is the Screaming Death, who has returned seeking vengeance. The Screaming Death happened to be digging shafts underneath the island that were large enough to cause the islands to collapse into the sea, forcing dragons to abandon their homes. The teens have to stop the Screaming Death before it causes Berk to collapse.