In a dystopian future where music is deemed illegal, AKB0048, successors to the idol group AKB48, rebel against the government to bring music to people's hearts. In the year 0048, three thirteen year old girls, Nagisa Motomiya, Orine Aida and Yuuka Ichijō, decide to audition to become members of AKB, although Nagisa has trouble singing due to the restrictions placed upon her by her father. As the girls hear they've passed the first round of auditions, Nagisa becomes downhearted as she wouldn't be allowed to go. However, after hearing about Yuuka's and Orine's reasons for wanting to join AKB, Nagisa decides to join Yuuka and Orine and head off to the auditions.

As Nagisa, Orine and Yūka travel on the ship headed for the auditions, they meet fellow auditioners Suzuko Kanzaki and Makoto Yokomizo, along with a stowaway named Sonata Shinonome. They soon learn that Chieri Sono, the daughter of a corporate CEO who had introduced them to AKB in their childhood, had apparently run away from home and boarded the ship to the auditions. Whilst searching for her, Nagisa encounters a strange kid who tells her she should turn Chieri in if she wants to survive the auditions. Just then, the ship comes under attack from the anti-entertainment force DES who come to capture the auditioners. Just as the girls are about to be captured, AKB0048 arrive to take on the forces. As Nagisa gets caught whilst retrieving a ribbon her mother gave her, the kid from before rescues her, revealing herself to be none other than Chieri. Chieri gets trapped under a chandelier, but Nagisa refuses to leave her behind.

As all the applicants are gathered, they begin intense idol training which, to their surprise, involves combat skills and self defense. The manager, Tsubasa Katagiri, reveals that, in order to be selected, the applicants must protect AKB during a guerilla concert. As Nagisa and Yūka argue about Chieri's change in attitude, they stumble across AKB0048 practising and learn how hard they practise and how their occasional squabbles help improve each other. The day of the concert come and the applicants find themselves up against the DES, with many of the girls failing under pressure. As Nagisa and Chieri fight together, Chieri gets shot whilst protecting Nagisa. Thankfully, it is revealed the DES attack was simply a simulation using paint balls. Having taken note of their friendship and teamwork, Tsubasa announces that Nagisa, Chieri, Yūka, Orine, Suzuko, Makoto and Sonata have all successfully passed and will become the 77th generation understudies.

As the 77th gen trainees arrive on Akibastar, they are brought to see an AKB concert, which is opened by the two remaining 75th gen trainees, Mimori Kishida and Sonata's older sister Kanata. However, Kanata is not too pleased that Sonata had joined up and ends up arguing with her. Speaking with Mimori, Kanata reveals she joined AKB so she could get revenge on the DES for killing her father and did not want Sonata to face such danger. As dance lessons begin the next day, Kanata becomes frustrated when her instructor criticises her lack of motivation and runs off. However, Mimori reminds her that it is okay to enjoy singing and she soon makes up with Sonata.

As the trainees are given a day off from their lessons, the girls split off into various groups doing various activities with their seniors. Nagisa decides to follow Chieri as she goes shopping, where they meet up with Yūko, who tells them about the last successor of Atsuko Maeda who disappeared during a concert. Meanwhile, Suzuko and Sonata becomes curious about AKB0048's producer, Sensei-Sensei, whilst Yūka and Orine meet with Tomomi Itano and her ancestors. As all of the current members teach the trainees about what gives them inspiration, Nagisa and Chieri decide to follow in Yūko's footsteps.

The trainees are to make their public debut at a handshake event in order to make a strong impression on their fans. As the girls have trouble deciding what to wear for the event, Orine, who wants to succeed Sashiko receives a hateful video mail, threatening to bomb the event if Orine doesn't quit, which leaves her shaken up. After some advice from Minami Takahashi that there will always be haters, Orine decides to attend the event. Despite still being a little shaken, she cheers up when she meets her first fan. Just then, as the kid from the video threat shows up, an explosion goes off, though it turns out to not be because of him, but instead a DES attack. As the others fight off the DES, Orine vows to protect her hater so she can learn how to improve herself, before they are backed up by the Ota, fans who fight alongside AKB in times of need. Afterwards, Orine receives another letter from her hater offering compliment and constructive criticism.

With some of the AKB successors attending a peace ceremony, Kanata, Mimori, Chieri and 76th gen understudy Megumi are chosen to be stand-ins for the next concert. As Chieri's standing in for Yūko invokes jealousy from the 76th gen understudies, they dig up dirt on how her father is a manufacturer of DES weapons. Chieri explains to Nagisa about how she ran away from home when she heard her father's machines were being used by DES. As Kanata chases after Chieri, reminding her that her father should not affect her dream, Minami, Yūko and some other successors who believe Kanata should be made into a successor follow Tsubasa to where she meets Sensei-Sensei. There, they discover a cave full of Kirara, which shows a mirror of who succeeds the original AKB48 member, predicting Kanata will succeed Minami, who does not take it well.

Following the stand-ins concert, Kanata, Mimori and the 77th gen understudies are asked to stand in for a guerilla concert on a planet where the entertainment ban is in full effect, prompting some jealousy from the 76th gen understudies. Meanwhile, Minami is still concerned about what she saw the other day, and acts weird around Kanata. As they make over there, Sae Miyazawa, a former 76th gen understudy, grows concerned about Megumi. As the increased security evokes debate about whether the concert should be cancelled, the ship comes under attack by the DES. Noticing Minami is struggling to stay focused, Yūko and Kanata set off to rescue her as she is overwhelmed by the enemy. As she recovers from her injuries, Minami laments that she does not want to graduate, but she does not want to hold Kanata back either. As Yūko tells Minami that she should focus on her dream above others, Kanata resolves to become stronger.

Due to Minami's injuries, Kanata is asked to fill in for her in an upcoming concert on the snowy planet Thundristar, much to Minami's dismay. As the understudies explore the planet and see how people under the entertainment ban are like, they meet a group of young fans who are looking forward to the concert. As Nagisa sings to cheer them up, Tsubasa decides to hold a multiple co-ordinated concert with the understudies in order to distract the DES whilst the main concert takes place. Before the concert begins, Minami demands to participate despite her injuries, much to Kanata's disappointment. As Kanata escorts Minami after she comes down with a fever at the end of the concert, Minami understands a bit more about Kanata's passion and once again feels she deserves to be Minami more than herself.

Following a meeting with Sensei-Sensei, Tsubasa announces a gravure shoot for all the members, including the understudies. As they arrive on the ocean planet Atamistar, Makoto grows concerned about her appearance, so Suzuko uses a technique to push all the fat up to her breasts. Meanwhile, Yūko confronts Tsubasa, who was a former AKB successor, about the reason why Atsuko disappeared and the center position was abolished, but gets no answers. As Makoto's plan ultimately fails after being stun by a jellyfish, the Kirara glows brightly when Nagisa and Chieri are shot together. As Suzuko explains to Makoto about how she'd rather be an administration member than a successor, Chieri tells Nagisa that she thinks Kirara has chosen her. Meanwhile, Tsubasa meets up with the camerawoman, the former successor of Minami Minegishi and a former Center Nova, who shows Tsubasa the picture of Kirara glowing for Chieri and Nagisa.

Following one of AKB's concerts, it's suddenly announced that the understudies will make their debut performance on Lancastar, Nagisa, Orine,and Yūka's home planet. As the setlist is announced, it is revealed Nagisa will performing a solo song generally sung by those who receive promotions. Meanwhile, Yūka grows concerned when she learns the boy she fell out with back home, Mamoru, doesn't want her to come back. It is soon announced that a new song has been composed by Sensei-Sensei for the understudies, the first since Atsuko's disappearance, irritating Yūko who becomes determined to learn this song herself. As they approach Lancastar, they learn DES have learnt of the concert. As the understudies explore the town and find the school has been abandoned, they encounter Mamoru and his comrade Aoi, who are members of the Entertainment Liberation. They explain what had happened during the past few months, including the arrest of Nagisa's father.

Nagisa, Chieri and Orine manage to evade capture until they are rescued by the WOTA, who offer to help Nagisa rescue her father. Arriving at the detention center, Kanata and Yūka join the WOTA forces in diversionary tactics whilst the rest of the understudies sneak in underground. However, Nagisa's father refuses to be rescued and they are forced to retreat empty handed. Whilst recouping at Yūka's family restaurant, Nagisa hears from Yūka's parents how her father was arrested because he didn't want Nagisa to be forced to quit AKB0048. Due to all the stress she has been feeling, Nagisa ends up losing her voice, so Chieri decides to fill in for her song. Meanwhile, Minami confesses to Yūko that she intends to graduate after the concert, whilst Chieri tells Nagisa not to think about quitting until after their performance.

As Tsubasa recalls some things Atsuko taught her, the understudies, along with the successors, request that they resume the concert. Just then, everyone hears the voice of Atsuko, whose light brings the concert to the detention center. As Chieri offers Nagisa the chance to sing, she gets her voice back upon seeing her family support her and Chieri's Kirara splits in two. The understudies' group performance soon begins, with everyone bathed in a radiant glow as they perform. As Minami fights to protect the understudies from the DES, the Kirara in the holy grounds choose her as Takamina's successor once more, whilst Sensei-Sensei prophesises that one of the understudies will become the next Center Nova. The camerawoman, who was the former successor of Minami Minegishi, predicted that if they glowed brighter, they would disappear. But didn't at the last minute, she falls on her feet, wondering about the Center Nova.