Little time has passed since the Magic Knights’ final confrontation with Princess Emeraude’s Mashin. Still haunted by the princess’ death, Hikaru Shidou returns to Tokyo Tower. There, she meets her friends Umi Ryuuzaki and Fuu Hououji for the first time since their spontaneous quest to save Cephiro. Plagued by nightmares of the realm she had left behind, Hikaru is relieved to find that her companions too want to return and serve the kingdom they once so dutifully protected. The Magic Knights’ wish is answered, for at the top of Tokyo Tower, the three are blinded by the same great light they had seen on the day they first met. Once more on the back of a flying fish, the group returns to Cephiro—a world now desolate and in ruins. With the collapse of the Pillar's power, monsters freely roam the land while three nations seek to annex Cephiro with hopes of seizing the Pillar for themselves. Complicating things further is the mysterious Lady Debonair, who proclaims herself to be the rightful heir of the fallen country. Now confronting graver stakes and radically different enemies, the three Magic Knights set forth once more to save Cephiro and bring peace. With the bonds they have forged together, the trio stands united in the face of such a great challenge.

After a daring escape from the Memory Museum, Sayaka Miki returns to Mitakihara City with unsettling news. Troubled by what she has learned, Sayaka reveals to Madoka Kaname and Homura Akemi the whereabouts of Mami Tomoe—but more importantly—the disturbing truth behind the existence of magical girls. Despite knowing the cruel fate that awaits them, the three quickly resolve to work together and save Mami once and for all. Meanwhile in Kamihama City, Yachiyo Nanami hunts various rumors in search of Hotel Fendt Hope, the headquarters for the Wings of Magius. The magical girl organization is Yachiyo's only lead in finding Iroha Tamaki, whose disappearance remains shrouded in uncertainty. Determined to reunite Team Mikazuki Villa, Yachiyo swears to destroy the Wings of Magius and put a stop to their insidious plans. Amid the turbulent situations, a calamitous threat approaches, presenting a dire conflict set to jeopardize the entire world.

Rumor has it that if a young girl strikes a bargain with a white fairy, it will grant any wish her heart desires. However, in exchange, she will become a magical girl and must put her life on the line to slay fearsome and ferocious witches. Iroha Tamaki, a kind-hearted middle schooler from Takarazaki City, is living proof that these rumors are true. Armed with a magical crossbow and the ability to heal injuries, Iroha seeks out the labyrinths where witches hide and defeats them before they can prey on humans. Yet Iroha has no memory of her wish, and even Kyuubey, the white fairy himself, seems to have no idea what Iroha requested of him. One day, Iroha hears rumors of a city where magical girls can be saved, and finds herself on a sunset train to Kamihama City. Unfortunately, she discovers that the witches in Kamihama are far more powerful than usual. After veteran magical girl Yachiyo Nanami is forced to save her, Iroha vows to never return. But when a chance encounter with a tiny Kyuubey seems to trigger distant memories, Iroha is compelled to investigate the mysterious city despite the danger.

The desperate battle in Kamihama City continues to intensify. With Walpurgis Night changing course for Mitakihara City, all eyes shift toward Embryo Eve—an artificial being, currently dormant, that can allegedly liberate magical girls from their destinies. As the Wings of Magius grow dangerously close to executing their plan, Iroha Tamaki's last chance to stop the organization is quickly fading. Despite the dwindling odds, lingering hope for the dawn of a better future invigorates her final endeavor, while also uncovering memories of a story tampered with by the hands of fate.