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In Ireland in 1650, the residents of the town of Kilkenny are working to clear the nearby woods under orders from the authoritarian Lord Protector, putting them at odds with a wolf pack who have been terrorizing the villagers. English hunter, Bill Goodfellowe, with his rebellious daughter Robyn, has been summoned to Kilkenny by the Lord Protector to exterminate the wolves. Bill goes out into the woods to place traps for the wolves, leaving his daughter alone at home. Wanting to help Bill, Robyn secretly follows him with her pet falcon, Merlyn, in an attempt to kill a wolf. However, she soon finds herself in the middle of the wolf pack's raid on farm sheep. After accidentally shooting Merlyn with her crossbow while trying to kill a wolf, Robyn watches a mysterious girl take him into the woods and follows them. Upon finding Merlyn miraculously healed, she is startled into a trap when one of the wolves confronts her. The wolf begins trying to help her escape, but she mistakes this for aggression and tries to fight it, causing it to bite her. Once out of the trap, Merlyn and the wolf lead Robyn to the wolves' den, where she discovers the wolf is the same girl from earlier. The girl, Mebh, explains she is a “Wolfwalker”, whose spirit leaves her body and becomes a wolf when she sleeps. Robyn comes to befriend Mebh, and also learns that her dormant mother Moll's spirit has not yet returned in her search for a new home for their pack, leaving Mebh alone to take care of them. Returning home, Robyn tries to convince Bill of the existence of Wolfwalkers, but he instead scolds her for going into the forest, and insists that she take up work to occupy herself.

The next morning, while working at the scullery, as ordered by the Lord Protector, Robyn is drawn into his chambers by a mysterious voice coming from a concealed cage, but is soon ushered out by the head maid. That night, as she sleeps, Robyn discovers her soul has left her body and has become a wolf. Shocked and confused, Robyn returns to the woods where Mebh reveals her bite has turned Robyn into a Wolfwalker like her, and helps her get accustomed to her new form. Upon returning to Kilkenny, Robyn is drawn into the Lord Protector's manor where she finds Moll's wolf form inside the cage. Moll tells Robyn that Mebh and the pack must leave the forest, as the Lord Protector plans to burn it down to wipe them out. The Lord Protector, seeking to restore control of the town, assures the townspeople that he can tame the wolves, and by extension, nature itself. He ignores Robyn's pleas to let Moll go and demotes Bill for failing to eliminate the wolves.