In late medieval Japan, Kai is a half-Japanese, half-English outcast who lives in the Akō Domain, which is ruled by the benevolent Lord Asano Naganori. When Kai was young, Asano found him lost in the forest and accepted him into his household. Kai and Asano’s daughter, Mika, eventually fall in love despite Kai being scorned by her father’s samurai due to his lowborn status and mixed ancestry.
Before a planned visit from Shogun Tokugawa Tsunayoshi, Asano is visited by the Shogun’s master of ceremonies, Lord Kira, who wants to take Akō for himself. Kira enlists the help of a shapeshifting Kitsune named Witch who sends a Kirin to kill Asano in the forest of Ako. Asano’s samurai struggle in their battle with the monster so Kai joins in riding an abandoned horse. As the monster charges him, Kai recovers a lost sword that he uses to slay it. Shortly thereafter he spots a white fox with different coloured eyes watching from the underbrush—Witch in her fox form. Later during the Shogun’s visit, Kai sees that one of the Shogun’s concubines has the same multi-colored eyes, leading him to assume that she is the fox from the forest. He tries to warn Asano’s principal counselor and samurai, Oishi, that she is a witch but Oishi doesn’t believe him.
Later, Kira arranges a duel for the entertainment of the Shogun: Kira’s best warrior, the giant Golem Samurai, will battle a warrior of Asano’s choosing. However, before the duel begins, Witch uses her magic to incapacitate Asano’s combatant. Kai secretly dons his armor and fights in his stead, but his disguise is revealed and the Shogun orders him severely beaten as punishment. Later that night, Witch uses her magic to make Asano believe that Kira is raping Mika, causing him to attack an unarmed Kira in his delirium. Asano is sentenced to death for attacking a Shogunate official (which is a capital offense), though the Shogun allows him to die with honor through seppuku. The Shogun then gives Kira both the Akō domain and Mika, although he grants Mika one year to mourn the death of her father before marrying Kira. The Shogun also brands Oishi and his men ronin and forbids them from seeking vengeance for Asano’s death. To ensure that the ronin do not interfere with his takeover plans, Kira imprisons Oishi in an outdoor pit to break his spirit.
Nearly a year later, Oishi is released by Kira’s men. He now knows that Kira is guilty of treachery for using Witch’s sorcery to cause Asano’s downfall. Oishi reunites with his family and asks his son Chikara to aid him in reuniting the scattered ronin. They learn that Kai has been sold into slavery and Oishi rescues him from the fighting pits of the Dutch colony of Dejima. Kai leads them to the Tengu Forest, a mystical place he escaped from as a child, so that they can find swords for themselves. Kai instructs Oishi to never draw his sword while in the Tengu temple and continues alone to another room to face the Tengu Master, who once trained Kai in their fighting ways. While Kai confronts the Tengu Master in a battle of wills, Oishi watches an illusion of his men being slaughtered by the Tengu, during which he fights the urge to draw his own sword. With Kai and Oishi both successful in their Tengu challenges, the ronin are given Tengu swords.