Beneath the fictional town of Arcadia lives a secret civilization of trolls, which humans are oblivious to. The trolls’ common enemy are the Gumm-Gumms, evil trolls from the Darklands, whom the trolls’ chosen warrior, known as the “Trollhunter”, is supposed to protect them from, among other dark miscreants.
Fifteen-year-old James “Jim” Lake Jr and his friend Toby find a mystical amulet which grants him the Trollhunter mantle. He is shortly approached by his new troll mentors, Blinky and AAARRRGGHH!!!. Despite his initial reluctance of leading two difficult lives, he eventually accepts his role after discovering that neglecting the amulet will nevertheless lead to its return. During his visits to Heartstone Trollmarket, the presence of the first human Trollhunter stirs resentment, but he quickly gains their honor. Throughout his training and missions, he befriends a gnome (which Toby dubs “Gnome Chomsky”) and discovers that goblins and Changelings (human-morphing trolls that replace humans to spy) are gathering for the completion of Killahead Bridge, which will be a portal for the Gumm-Gumms from the Darklands – the project is being lead by Bular, the son of the Gumm-Gumm’s leader Gunmar, and the Changeling replacing Jim’s high school teacher Mr. Strickler.
While discovering more mysteries, he is forced to reveal the truth about his life to Claire Nuñez when she becomes a target of the goblins. After he, Toby, Blinky, AAARRRGGHH!!! and Draal infiltrate the gathering and destroy the bridge, Jim is forced to battle Bular and eventually kills him. He returns to Trollmarket, where the citizens celebrate Bular’s defeat.
Shortly afterward, Claire proposes a quest into the Darklands to rescue her baby brother Enrique, who has been replaced with a Changeling who they dub NotEnrique. Blinky informs them that the only way out of the Darklands is to kill Gunmar – the only way to destroy him is with the three Triumbic Stones. After finding the first two, their enemy Strickler frees ancient troll assassin Angor Rot from his bonds – using Angor’s ring, he forces him under his control. After Jim indirectly causes his ring to break, Angor goes on a rampage, attempting to kill Strickler and Jim – in the process, Strickler and Jim’s mother are injured. Trollmarket’s leader, Vendel, informs Jim that the only way to cure it is to break the binding spell that ties his mother’s and Strickler’s fates together – however, his mother’s memories of the troll world are erased. Strickler hands Jim the last Triumbic Stone.
Angor Rot begins to invade Trollmarket after stealing the key from Toby and Claire. They defeat him. During his rampage, unfortunately, AAARRRGGHH!!! died because of the potion, much to the grief of the group, especially Toby. Thinking that he was responsible for the death and the endangerment of his friends, Jim sets off to the Darklands alone, not wanting to lose any more of them.
