25 years before the start of the series, massive creatures known as Dragons began appearing around the world, causing widespread destruction before vanishing. Shortly afterwards, humans with powers similar to that of Dragons were born and came to be known as D. At present day, the world's only male D, Yuu Mononobe, is transferred to Midgard and encounters a naked girl, Iris Freyja, at the beach. Iris mistakes him for an intruder and unsuccessfully tries to attack him, but then loses consciousness due to her attack backfiring and is saved by him. While the two talk, Yuu is approached by his sister, Mitsuki Mononobe, who announces to him that he will be a Midgard student henceforth.

Loki tells Yuu that it is his duty to prevent the girls at Midgar from becoming dragons and to kill them if they do. Iris has been having suicidal thoughts as she is dangerously close to becoming a dragon, but Yuu convinces her to think about living. The girls prepare for combat as Leviathan approaches the island.

While the girls are fighting Leviathan, NIFL soldiers attack Iris to stop her from becoming a dragon. Yuu protects Iris by defeating the soldiers using his dark matter guns. The girls penetrate the barrier with a coordinated attack and Yuu destroys Leviathan using the Babel cannon with Iris supplying dark matter to power up the attack.

Tear enrolls at Midgar Academy and claims Yuu as his wife as he was the person who saved her life when a fire burned down her home.

Tear's background is revealed as her family was killed when a dragon cult led by Kili burned her home and killed her parents. Tear takes pride in being a dragon because the cultists hold her in high regards, but Yuu convinces Tear to live as a human rather than a dragon. Kili arrives at Midgar to initiate an attack to take Tear away with her.

Kili attacks Midgar with the dragon Hecatoncheir that can regenerate. While Lisa looks after Tear, she is attacked and overpowered by Kili. Wanting to protect her friends, Tear agrees to go with Kili and become the Basilisk's wife. But Yuu convinces Tear not to go with her while he awakens the power of Leviathan to defeat Kili.

Kili retreats after being defeated by Yuu. Yuu devises a plan to defeat Hecatoncheir by drawing it out to sea where he could use Babel without causing any collateral damage to Midgar. Yuu uses an anti-gravity bullet to lift Hecantoncheir into the air and the girls generate a wind to blow it out to sea. The girls weaken Hecantoncheir's barrier and Yuu destroys it using Babel with Tear supplying the dark matter.

With Basilisk headed towards Midgar, Class Brynhildr heads to an uninhabited island to draw Basilisk away from Midgar knowing that it is after Tear. On the way to the island, Mitsuki and Lisa are at odds with each other over Miyako's death. Mitsuki explains her relationship with Miyako to Yuu. She was very close friends with Miyako, but she became a dragon when the Kraken invaded Midgar. Miyako ordered Mitsuki to kill her and Mitsuki reluctantly complied. With Yuu's help, Mitsuki and Lisa make amends with each other.

After the Dylan's plan has gone awry, the execution of a new operation is entrusted to the Midgar. Having analyzed Basilisk's third eye, Haruka gives an overview of the new strategy to the students of class Brunhild, which is to form pairs and launch a strike on Basilisk, by infiltrating the volcanic island. She orders them to carry out the attack before the catastrophe beam can be fired. For this operation, the pairs consist of Yuu and Iris, Mitsuki and Ariella, Lisa and Ren, and Firill and Honoka. Yuu uses the dragon ability "anti-gravity", and he has a flashback to the time he was told by Charlotte that Mitsuki also has something akin to his power.

With the students in the catastrophe beam's line of fire, Honoka uses her power to get Yuu and Iris below the beam, while Yuu fires an anti-gravity bullet to direct the beam safely into the sky. The island is destroyed by Basilisk and students retreat back to the ship. After analyzing the attacks, Yuu determines that its third eye cannot fire the catastrophe beam in quick succession and its discharge time is five seconds. As such, Yuu comes up with a new strategy that involves dropping Mistilteinn, but with the students using dark matter to protect the Mistilteinn from the third eye's catastrophe beam for five seconds.

Yuu defeats Kili in a fight to decide Tear's fate. As part of the agreement, Yuu's plan to destroy Basilisk goes forward and Yuu orders Kili to live on as a human. Kili kisses Yuu as she leaves asking him to show his superiority by defeating Basilisk. Mitsuki devises a strategy to defeat Basilisk with all possible fallback scenarios planned out. The students drop with the Mistileteinn and protect it from the first catastrophe beam discharge by Basilisk's third eye, but with the discharge having come much sooner than anticipated that the third eye had time to fire the catastrophe beam a second time, which destroys Mistileteinn. However, the blast creates an opening for the students to disable the third eye and immobilize Basilisk, allowing Yuu to destroy Basilisk using Babel. The students return to Midgar as Mitsuki's outlook on life has changed to a more optimistic one and Yuu tells Iris about his memory loss as a condition for using Babel, and Iris vows to stay with him.