Fifteen years after Nobunaga Oda’s defeat at the end of Onimusha 3: Demon Siege, the former vassal Tokichiro Kinoshita rises again under a new name, Hideyoshi Toyotomi, uniting Japan and bringing the Sengoku era to a close. Yet the fragile peace shatters when the sky is split by the ominous “Omen Star.” A wave of natural disasters follows, and Hideyoshi mobilizes his armies to strike the mainland Asia while the Genma reemerge from the shadows. In this new age of upheaval, Hideyoshi wields Genma power to tighten his grip, while a strange collection of cherry trees is ferried toward Kyoto. Among the upheaval stands a stubborn thread of resistance: Hideyoshi’s illegitimate son, Soki, also known as Yūki Hideyasu, refuses to bow to his father and fights under a stubborn alias, accompanied only by a bagworm named Minokichi.
Driven by a personal code and a fearsome reputation, Soki spends two brutal years raiding transports bearing the Genma-tended trees, a campaign that earns him the nickname “Blue Demon.” Along his path, a chance encounter brings him into contact with a formidable ally: Jubei Yagyū Akane, a young clan member who inherited Oni powers from her grandfather. Jubei joins forces with Soki as they work to pierce the fortress where the trees are prepared for Kyoto’s journey, and their alliance deepens as they uncover that the trees are Genma structures built from human bodies. The Genma insects within threaten to seize control of anyone who ingests them, turning people into vessels for their dark purposes.
The team’s path crosses with another enigmatic figure, Tenkai Nankobo, a monk who has hunted for the bearer of a potent Oni power—the “Black Oni.” Wearing an Oni gauntlet, Tenkai joins the quest as the group pushes toward Mitsunari Ishida’s castle in a bid to disrupt Hideyoshi’s broader scheme and rescue a Spanish missionary, Roberto Frois, whose own history with Luis Fróis reveals layers of alliance and betrayal involving the Genma. During these trials, Soki’s attention is drawn to a mysterious man dressed in white, a shadowy presence that seems to surface whenever the fight sharpens.
As the party advances, Ohatsu—a childhood friend—enters the fray, and Munenori Yagyū’s manipulations pull her toward his side even as Soki’s suspicions about Hideyoshi grow stronger. The quest intensifies when Jubei’s and Roberto’s captures threaten to fracture the effort, forcing Soki to press on toward the looming Mother Genma Tree in Kyoto. The mission sparks a tense arithmetic of loyalties, and Ohatsu’s loyalty is tested as Munenori presses her to stand by him. With Jubei and Roberto temporarily out of reach, Soki heads to confront Hideyoshi alone, while Tenkai, Ohatsu, and the others rally to a crucial turning point in the struggle.
Sacrifices and revelations abound as the party reaches a Genma laboratory where the scheming Triumvirate—Claudius, Rosencrantz, and Ophelia—seek to resurrect their god. A fateful confrontation with Sakon Shima, a brainwashed warrior, punctures the illusion, and Roberto’s desperate actions threaten to topple Hideyoshi’s power by destroying a Dark Stone powering him. Yet Ophelia, inhabiting Lady Yodo’s corpse, reveals the depth of the Genma’s reach, and the team must push through grief and deception to press on.
Guided by Tenkai’s wisdom and Ohatsu’s steadfast courage, Soki and Jubei press toward the final confrontation in Kyoto. Along the way, Minokichi makes a final sacrifice to buy time for the group to reach their goal. Once in Kyoto, the city is enveloped in Genma energy as the group fights the resurrected Triumvirate and the Genma forces behind them. Jubei battles Munenori, who invests enough Genma insects to empower himself with both Genma and Oni blood, while Soki confronts Hideyoshi, who carries the Genma Seed that could unleash the god’s return. When Hideyoshi is defeated, Ophelia is destroyed, and the Genma’s threat intensifies as Fortinbras—now the Genma Lord—reappears, having been resurrected by Munenori and the white-clad figure who has haunted Soki’s steps.
The battle unfolds with a heavy cost: Munenori, consumed by ambition, is slain as Fortinbras, the ultimate Genma foe, rises. Soki accepts his fate and ascends toward the Omen Star, only to be called back by Jubei, who pleads for him to remember life beyond victory. Near the top, the barrier closes around them, and Soki shares a bittersweet moment with Jubei before stepping into the impossible. He disappears into the Omen Star, dying as the blossoms of Kyoto return to life and a tenuous peace settles over the land.
In the aftermath, the world begins to heal. Ohatsu chooses a new life with a different family, tending to her young nephew and maintaining the memory of those lost. Roberto returns to his homeland to ensure Genma power cannot take root there again. Tenkai departs with Arin—the tengu who hints at a deeper history with Samanosuke Akechi and Ako—into parts unknown. Samanosuke, aged yet preserved by the Oni gauntlet’s power, remains an enduring symbol of the past, while Ako hints at a continuing bond. Jubei, having never returned to the Yagyu village, visits Soki’s grave and then sets out on a new journey to seek meaning in life, a personal quest sparked by the sacrifices and victories of the days that followed the Omen Star.