Iroha Tamaki, a Student in Takarazaki City, has been battling Witches as a Magical Girl. However, Iroha can't seem to remember the wish she made when she became a Magical Girl. One day, she hears a rumor from another Magical Girl, Kuroe, that Magical Girls can be saved if they go to Kamihama City. During a battle with a Witch, Iroha unexpectedly finds herself in Kamihama but…

Iroha remembers that her wish was to cure her younger sister, Ui’s, illness; however, there is no sign of Ui’s existence in her life. She goes to Kamihama City to find clues about her, but is attacked by a Witch and subsequently saved by a trio of Magical Girls, Momoko, Rena, and Kaede. There is a rumor going around about the Friendship Ending Staircase at Rena and Kaede’s school. Momoko and the others believe that a Witch is involved in the rumor, so they’ve been investigating it, but…

Rena wrote Kaede's name on the Friendship Ending Staircase. Kaede apologizes to Rena, but she is kidnapped by the Chain Monsters, confirming that the rumor about the staircase was true. In order to find Kaede and bring her back, Momoko and her companions come up with a strategy to lure out the Chain Monsters. Yachiyo has joined the group after being asked by Momoko to help them. Yachiyo claims that Iroha will hinder the operation and refuses to let her participate in the battle with the Chain Monsters.

Iroha decides to investigate Kamiahama City’s rumors in order to find clues about her missing sister, Ui. Mitama introduces Iroha to Tsuruno, the daughter of the owner of a Chinese restaurant called Banbanzai. Tsuruno asks someone who is familiar with the rumors to help investigate, but Yachiyo is the one who shows up at the meeting spot. Tsuruno says Yachiyo is knowledgeable about the rumors of Kamihama City. The three suspect that the Séance Shrine may have something to do with Ui’s disappearance…

At the Séance Shrine, Iroha wrote her sister's name, Ui, and Yachiyo wrote the name of her former best friend, Mifuyu, on votive plaques. As if to confirm the truth of the rumor, Ui and Mifuyu appear, but they are twisted imposters of their loved ones. Iroha and Yachiyo are attacked by the fake Mifuyu and the master of the Séance Shrine, a Horse Monster, and find themselves in a bind that threatens to end their lives. Iroha's Soul Gem gets cloudy, making her slowly lose consciousness. What sort of transformation will she undergo?

Iroha wanders into Kosho Ward in Kamihama City. On the street, she is offered some Lucky Owl Water, which is said to bring good fortune, and without much thought, takes a sip. Another Magical Girl named Felicia also happens to drink the Lucky Owl Water. Wherever they go together they have extremely good luck. They have such good luck, in fact, that Iroha finds it a little strange. Felicia makes a living as a mercenary, and offers her services to Iroha to help find Ui, but…

Felicia was asked to join the Wings of the Magius, an organization that works within the shadow of rumors. She betrays Iroha and her friends and joins them. Kyoko is also invited by the Wings of the Magius and decides to join the organization. Iroha and company track Felicia down to an underground waterway, where the Wings of the Magius lurk. When the good luck count from the Lucky Owl Water reaches zero, it is said that unimaginably bad luck will befall whoever drank it.

Iroha moves into Mikazuki Villa and transfers to Kamihama City University Affiliated School. She discovers that even though Kaede goes to the same school, she is unable to contact her. Iroha has a hard time getting used to her new surroundings, so when she sees that Rena doesn't have many friends in class, they decide to eat lunch together on the rooftop. Iroha is still gathering information about various rumors, and Rena tells her about the rumor of the Invisible Girl and Endless Solitude. Tsuruno hears about the rumor of the Radio Wave Girl from a regular at Banbanzai and tells Iroha about it.

Iroha is convinced that all rumors are connected, so she decides to reply to the spam messages that are being repeatedly sent to her. The one who has been sending the texts calls herself Ai, and she asks Iroha to come to Endless Solitude to delete her existence. However, Sana Futaba, who is a captive in Endless Solitude, seems to be satisfied with her life there.

Ai decides to disappear in order to free Sana. Alina is infuriated by the destruction of Endless Solitude and goes into full attack mode against Iroha and her friends. They find out that the Magius have been using the Uwasa's territory to confine and raise Witches. Iroha and company fight an uphill battle, but Mami and Mifuyu appear on the scene to put an end to Alina’s rampage.

A student at Mizuna Girls' Academy, Tsukuyo, is hiding the fact that she is a member of the Wings of the Magius. Iroha goes to see Tsukuyo and asks to be introduced to Nemu Hiiragi, a friend of Iroha’s sister, Ui. Tsukuyo promises to Iroha that she will talk to Mifuyu about the matter. Sana has gotten accustomed to living at Mikazuki Villa, and suggests to everyone that they surprise Yachiyo with a gift, but…

With Yachiyo in low spirits, Iroha and company leave her behind and head for the Memory Museum. Touka Satomi, a friend of Iroha’s sister, Ui, awaits them there to give them a lecture about the truth of Magical Girls. Yachiyo’s past memories give her a push, and she decides to go find Iroha. However, at that very moment Iroha is already in the midst of a "vicarious practical learning" course prepared by the Magius.

Iroha refuses to join the Magius. When she and Yachiyo meet up, she is eager to go search for Tsuruno and the other girls. However, Yachiyo believes that her wish brings tragedy to those around her and tells Iroha that she is disbanding the team. The Memory Museum begins to collapse. Iroha and Yachiyo try to escape, but Mami, who has become an entirely different person, attacks them.

Madoka and Homura fight an uphill battle against the Class Leader Witch. When the Witch’s minions attack Madoka, Homura stops time and uses a gun to save Madoka. However, the appearance of a mysterious girl takes Homura by surprise which breaks her spell to stop time. As the minions close in on Madoka, Sayaka returns from Kamihama City to save her from the impending crisis. Sayaka explains to Madoka and Homura what happened to Mami in Kamihama and the truth about the Magical Girls.

Yachiyo pursues Black Feather and the others to find Hotel Faint Hope, which is where the headquarters of the Magius is located. After battling the Uwasa of Peeking Castle Town, she walks through the shopping district where Uwasas have appeared before to find the entrance to Hotel Faint Hope. There, she meets a Magical Girl named Kuroe from Takarazaki City and small Kyubey, but Kuroe suddenly tries to run away. After chasing Kuroe, Yachiyo’s former best friend, Mifuyu Azusa, appears before her. Mifuyu explains that the methods of the Magius are necessary to prevent any more girls becoming victims like Iroha…

Yachiyo and Kuroe find Iroha inside the Labyrinth of the Uwasa of the Eternal Sakura. However, Yachiyo and Kuroe are swallowed by the Doppel of Silence that suddenly appears from Iroha’s body. When Yachiyo awakens, she finds herself at Mikazuki Villa eating breakfast with Tsuruno, Felicia, Sana, and Iroha, but Kuroe, who is not supposed to be there, is in the room with them. Yachiyo and Kuroe are baffled by the situation they are in, but they have a hunch that they are not in the real world, but in a dream world being shown to them by the Doppel of Silence. They are concerned about Iroha’s safety in the real world, so they do all they can to wake up Iroha in the dream.

Iroha hears about Nemu Hiiragi, the best friend of Iroha’s younger sister, Ui, from Kuroe. Iroha finds out that Nemu, who is also a member of the Magius, remembers her and asks Kuroe to take her to Nemu so they can talk. Iroha, Yachiyo, and Kuroe head to Hotel Fendt Hope, the headquarters of the Magius. When the trio arrive at Hotel Fendt Hope, they have an encounter with the Amane sisters. While Yachiyo distracts the Amane sisters, Iroha and Kuroe make their way into Hotel Fendt Hope to find Nemu, but they bump into Rena Minami and Kaede Akino, who are dressed as the Black Feathers.

Iroha embarks on a journey to find her friends from Mikazuki Villa. Kuroe is genuinely concerned about Iroha so she decides to tag along. Meanwhile, Felicia and Sana are working inside of the Magius as Black Feathers. Felicia proclaims that she will not return to Mikazuki Villa until she finds out how they can avoid becoming witches. Sana begins to question the actions of the Magius while she manages the people captured by the Uwasa,. Mifuyu, who is acting as a White Feather, finds herself in a predicament when she reunites with an unexpected person. Amidst the intricate tangle of everyone’s emotions, Touka announces her strategy to save all Magical Girls. What could it be?

Kuroe lets Iroha get ahead of her while fighting with Magius. Kuroe hears a whisper that puts her in a shock: “Did you forget about me?” At the same time, Iroha is hearing Ui’s voice. Felicia and Sana are confused about Magius’ plan. Sana has questions and explains her intent to Mifuyu, who seems to have given up on everything. Due to the plan, Yachiyo is after Iroha in Kamihama City, which is filled with a large number of Witches. While there, Yachiyo comes across a Magical Girl from Mitakihara City.

The Magical Girls break into the headquarters of the Magius. After Iroha and Yachiyo reunite, they meet up with Madoka and the other girls, but are confronted by Tsuruno Yui and Mami Tomoe who have become soldiers of the Magius. Mami and Tsuruno, who are being manipulated by another entity, begin attacking the Magical Girls. Iroha and Madoka are in a bind as they are unable to fight back. As a tactic, the Magius summon countless Witches to gather in Kamihama City. The largest ever Supercell is approaching and will hit Kamihama City in six hours. The true identity of the Supercell is actually Walpurgisnacht, the most sinister and evil Witch ever.

Tsuruno, who had merged with the Uwasa, is defeated, which triggers Touka from the Magius to direct her rage toward Iroha and her friends. Touka sends the Uwasa of the Soldier Bear army to attack them. Nemu is upset with Touka’s actions and at how things aren’t turning out the way she intended. Meanwhile, Iroha finds herself alone in a strange world. She is sitting in a seat in a theater where a Magical Girl named Mel is predicting the future. When Iroha sees Mel, she remembers the past events that Touka showed her at the Memory Museum.

It happened in the past… Iroha would go to the hospital daily and play with Ui, Touka and Nemu. The girls loved Iroha and looked forward to her visits. One day, the three girls create an Uwasa similar to an urban legend while playing. That way, if they died, the Uwasa they created would live on and remind Iroha of them. Iroha also created the “Uwasa of Eternal Sakura”, with the wish that the three girls will be discharged from the hospital without illness. And one day... Kyubey appears before Iroha.

The Magical Girls rush to Iroha while fighting against Uwasa of the Soldier Bear. The Amane sisters also stand in their way, but Mifuyu keeps them in check. "The plans of the Magius have failed." Meanwhile, Iroha and Touka regain the memories that Nemu's power took from them. Touka is happy to be reunited with Iroha but can’t recall why they became enemies in the first place. Nemu tells Touka why she had been hiding the truth until now. Now, they see the promise they made with Ui in a new light.

To fulfill their promise to Ui, Touka and Nemu set their plan in motion with Embryo Eve. Yachiyo desperately tries to stop them. As Alina watches events unfold, Kuroe is isolated and alone. And Kyubey is not far behind… Meanwhile, Iroha wakes up in her room at home. Everything looks the same as when Ui was still around. Finally, Iroha is reunited with Ui.

Iroha grieves about the battles that have been fought so far and figures she couldn’t save anyone in the end. Kyubey thanks Iroha and says that her hope caused everyone to fall into despair. The despair of Magical Girls is what Kyubey has been seeking all along. All the while, Iroha’s Doppel continues tormenting her. As a result of Iroha’s interference with the Magius, more Witches will be born. On the brink of despair, Iroha hears a familiar voice call out to her.