A skilled assassin named Tokaku Azuma is transferred into Myōjō Academy's "Class Black", tasked with identifying and killing a target amongst her twelve classmates, the rest of whom are also assassins. At her first homeroom class, consisting of five of the total 13 students, Tokaku finds herself drawn towards a kindly girl named Haru Ichinose, believing she may be the target. As Tokaku spends more time with Haru, who is revealed to be her roommate, she notices some knife wounds on her legs. After encountering her various classmates throughout the evening, Tokaku, who had also been tasked by her teacher, Kaiba, with solving a puzzle reading "The world is filled with (___)", becomes bewildered when Haru suggests "forgiveness" as an answer.

All 13 students are now assembled and things are about to get serious. But one of them thinks she can jump the gun and beat everyone to the prize.

Tokaku switches sides to Haru, but the game is still on and the first official Class Black assassination attempt is made.

It's three straight days of testing for Class Black. While Haru is intent on passing those tests, another one of the girls is intent on killing her.

Class Black prepares to put on a production of "Romeo and Juliet" for the school festival and another assassin tries her luck.

Class Black puts on "Romeo and Juliet" in front of a student audience, but with so many deaths in the play, maybe one or two will be real.

Another assassin tries her hand, but this one proposes a game with rules that will give Haru and Tokaku a chance to beat her fair and square.

The field has been whittled to four assassins. With classes done and a typhoon closing in, Haru and Tokaku are in for a harrowing evening.

It is shown that Tokaku's inability to kill came from her aunt, who followed her sister's wishes to not have Tokaku grow up to a killer like the rest of her bloodline. With Tokaku still locked in battle with Isuke, Haru attempts to escape from Shinya's violent mallet attacks on her own esteem. After receiving another message from Kaiba, Tokaku manages to stun Isuke with a taser hidden in her shoe and escape. However, she falls into a trap laid out by Isuke and is pushed off a bridge. Meanwhile, Haru is chased to the A/V room of the school, where Isuke uses a projector's light to cause Shinya to experience traumatic memories and knocks her out before turning her attention towards Haru. Tokaku, who had managed to survive her fall, finally comes to understands how her mother and aunt protected her with their lives and overcomes her hesitation, stopping Isuke and rescuing Haru. With both Isuke and Shinya defeated, the remaining classmate, Sumireko Hanabusa, prepares to make her move

With only Tokaku, Haru, Nio, and Sumireko remaining in Class Black, Sumireko gives Haru an invitation to a tea party, claiming it not to be an advance notice. Meanwhile, Otoya breaks out of prison and sneaks into the dorms to try and target Haru again, but is stopped by Sumireko, who crushes Otoya's scissors in her hand with little effort. Later that night, Haru and Tokaku arrive at the tea party, where they discover robotic puppets of all the other classmates, as well as the restrained Otoya. After explaining how she wants to prove she is a stronger "queen" than Haru, Sumireko delivers her notice and has her puppets attack Tokaku, giving her a selection of guns to fight against. After being prevented from separating herself from the others to target Haru, Sumireko reveals she has powerful robotic limbs and launches a fierce attack against Haru. In the ensuing battle, Otoya breaks free and manages to disable one of Sumireko's arms, only for her to replace it with another weapon, with Otoya once again captured by Nio. As Tokaku becomes cornered, Haru lures Sumireko away from her and uses her robotic limbs to her own advantage, knocking her off the side of a building. After receiving another text from Kaiba asking "Who is the queen?", Tokaku asks Haru what Sumireko meant by her words about her being a "queen bee", but Haru simply says it is not the time to tell her yet.

With all the other assassins defeated, Nio announces there will be an orientation held at midnight revealing the secret behind Class Black, implying that Haru already knows something. That night, Tokaku and Haru arrive at the orientation, where they are greeted by Yuri, who reveals Class Black was designed as a test to see if Haru could survive against twelve assassins and become a successor for her clan, who control most of the world. Yuri implies that Haru, consciously or not, allegedly has the power to manipulate and control others into protecting her, which Haru refuses to acknowledge. As Haru runs off in denial, Yuri asks Tokaku to think of a wish she wants granted for winning Class Black. That night, as Tokaku feels she had been manipulated the entire time, with no way for Haru to prove otherwise, Kaiba tells her that all of the riddles he had sent her have no "right" answers, tasking Tokaku with finding her own answers. Meanwhile, after Haru asks Yuri to let her leave the clan and live a normal life, Nio takes her to their clan's cemetery, which Myōjō Academy was built upon, giving her some time to reflect on things. After spending time with her family's grave, Haru is approached by Tokaku, who delivers her own advance warning and draws her sword against her.

As Tokaku begins her attack, Haru is suddenly dragged off by another Tokaku, who claims the other Tokaku is actually Nio using hypnotic suggestions to take on her appearance. The two Tokakus soon battle against each other with the real Tokaku managing to overcome her fake and stab her. Haru then charges against Tokaku, but ends up becoming stabbed herself, leaving Tokaku devastated, feeling the one wish she has can no longer be granted. As the end of the school year comes, it is revealed that both Haru and Nio had survived their attacks, with Haru becoming the sole graduate of Class Black. With all the other assassins returning to their regular lives, Tokaku sends one last reply to Kaiba before joining Haru in delivering everyone's diplomas. After the credits, Kaiba receives a text message and smiles, though the content of the message is not revealed.