In the cave, Hiccups finds Garff while Fishlegs brings the Cavern Crasher to help dig a new exit and move the Singetail eggs to safety. Gobber believes it to be the Lycanwing, a mythic dragon whose bite can turn humans into vicious dragon hybrids, and Snotlout preys on Tuffnut's paranoia making him believe he will become a Lycanwing by the next full moon. The riders return to the island and reclaim the hidden gold, and Heather finally decides to go with Dagur to find her father. DreamWorks' Dragons: Riders of Berk picks up where the feature film left off. Hiccup uses his flight suit to win the trust of the wild dragons and leads them in a counterattack that fends off Ryker and his group. Back at the Edge, Heather finds a note from Dagur telling the truth about their father, leaving Heather to mourn in silence.
They deliver the axe late only to discover a fight broke out and the wedding was cancelled. With the aid of Stoick and the Rumblehorn, the riders create a wall to block the wave and protect the island. The search for Oswald doesn't end on a happy a note, with Dagur only finding his remains and a last message to him and Heather, though he continues his father's work by helping the Sentinels defend Vanaheim from the rogue Grim Gnasher dragons, and leaves satisfied that his father passed proud. But when Alvin and Mildew help him discover what the Screaming Death has been after all along, he comes up with a plan to end the war between the Outcasts and Berk, stop Dagur, get rid of the Screaming Death, and save Berk once and for all. The four attempt to work together, but their efforts are hindered by Stoick and Spitelout's constant arguing, and their sons are left to reluctantly take their father's side. The twins hold a funeral for Macey back on the Edge, where Tuffnut reveals stolen schematics that leave the riders worried for what 'Project Shellfire' entails. Seemingly accepting that Ruffnut's place is with the Riders, Wingnut accepts Atali as its new Wingmaiden and caretaker.
After arriving, they find the Sentinels seemingly dead and interrogate a remaining Flyer, who reveals the rest of the Flyers are on their way to inform Johann of Vanaheim's location. The riders take it back and nurse its leg to health when Fishlegs discovers the Stinger has gained webbed feet as a result of evolution. Though Ruffnut struggles with the tasks to care for her Razorwhip, named Wingnut, she only succeeds thanks to Tuffnut's secret assistance. After discovering that the Bork notes are fakes made by the Outcasts, the duo tries to flee, but are captured by Alvin. Using a Skrill as a diversion, Hiccup and Viggo enter their headquarters where Viggo betrays Hiccup to earn favor with Johann and Krogan once more.
Meanwhile, Fishlegs discovers Dragon Root, which could end up affecting not just Stormfly and Hookfang, but all their dragons. Hiccup faces Johann alone while Toothless defeats Krogan and recovers the egg. It is up to Hiccup and his friends to convince him otherwise. Upon investigation, they discover it to be a young adult Seashocker having drifted into the cove after being separated from its pod. The Berk forces are quickly put on the defensive and Krogan takes the chance to launch all his Dragon Flyers against them, which ultimately leaves them defenseless when Hiccup returns to turn the tide.
A trade takes place, but Gustav decides to stay with Dagur. After hearing this, Astrid starts to think that Hiccup isn't interested in her anymore since they are not as publicly affectionate as Dagur and Mala and begins to question her relationship with him. The dragons bond and fly away, allowing the riders to return home. While Fishlegs is wrapped up in trying to beat Snotlout, Fishlegs fails to notice that Meatlug caught Outcasts sneaking into Berk, which leads to her being captured. Dagur leads Viggo's fleet away and swears to Heather that he will return to answer her questions, leaving his worried sister behind.
Upset over his father's lack of faith of him, Snotlout tosses the axe in anger down on an island where it is found stuck to the magnetic hide of a new dragon — the Armorwing. Though highly reluctant, Hiccup works together with Dagur to cure Toothless but the two are captured and Dagur appears to abandon Hiccup, but later comes back riding Toothless to save him. The dragons, being the wild beasts they yet remain, unintentionally stir up trouble time and again, leading to the more grouchy types among the Vikings to take exception to their presence. Snotlout is reassured that he will be great, but he will follow his own path instead of his father's. However, Mildew is also imprisoned as he's no longer of any use to Alvin now that he has Hiccup.
Fishlegs is reluctant to let the Seashocker leave in the interest of studying it, but is convinced otherwise after it is injured by Stormfly. DreamWorks Dragons was the first DreamWorks Animation series to air on Cartoon Network rather than. Meanwhile, the Wingmaidens entrust the egg with Valka, Stoick recovers from his injuries, Mala and Dagur are married, Fishlegs and Snotlout both begin courting Ruffnut, Hiccup decides to destroy both Dragon Eyes to prevent them from falling into the wrong hands and the Riders leave the Edge to return to Berk. Hiccup, Fishlegs, and the twins comes across a marble mining operation on a nearby island using trained Catastrophic Quakens, and while Fishlegs is determined to save them, Hiccup fears it may already be too late. Hiccup, after fiddling around with the eye, finds that it's activated by the fire of any Dragon and works as a light projector showing him maps, writing and Dragons he's never seen.
When they return, the riders re-welcome Heather while offering their support and she and Astrid take the time to bond. Hiccup also discovers a new series of lenses for the 'Dragon Eye'. With Spitelout's help, Hiccup discovers weaknesses in the Singetails' behaviours while the Riders, Stoick, the A-Team, and the Berk fleets launch a preemptive strike on Dragons' Edge where the Hunters are. While searching the island for more, they discover a group of hunters, who are following the teachings of his ancestor, Ingard Ingerman in trapping Dramillions and using them to help train new recruits. In the end, Heather decides to leave, saying she has much she needs to figure out.
The Speed Stingers have trekked across the frozen sea to Berk and driven everyone out of town. He asks for Hiccup's help in deciphering Oswald's diary, which contains a picture of a massive dragon skull that leads them back to Vanaheim. They suddenly realise that the Night Terrors, under the command of their Alpha, a white Night Terror, need to flock into a shape of a giant version of themselves or any other dragon they wish as a defense mechanism to scare off threats or predators. Together they meet with Johan who reveals Dagur's plans to purchase new dragon-proof ships and weaponry, and they convince the riders to launch a surprise attack. Snotlout and Gustav work together to free Dagur, but bit by bit under the gravity of the situation and Snotlout's pressure, Gustav's confidence wanes until he admits his cheating while under Dagur's tutelage. With the help of a wild Thunderdrum, Hiccup uses Monstrous Nightmare gel that Snotlout brought with him to warm the hardened mucus and free the group.