On Tokyo Jupiter, a 17yr old boy, name Ayato, is living a normal life until, Tokyo Jupiter is attacked. When Ayato is saved by Haruka, Ayato cracks an egg which released a structure, known as RahXephon, to fight against Mu.

Ayato is tested and found out to be normal, minus the symbol on his torso, Quon has one as well. While Ayato meets, Soyoko a co-worker and finds out he will be living with Haruko and her sister Megumi, and their uncle Rikudo. Meanwhile Itsuki finds out, that Quon is his sister. When Ayato is unpacking, he finds Buchi, which Quon packs for him. And after the dinner Rikudo gives Ayato a name plate.

14 Years ago a Dolem apppeared. Now the same dolem is back, and killing people in Australia. Kim Hotal get's an unauthorized sound bite due to the fact that Dolems use these sounds for their attack patterns! Now, Terra must wait for the Dolem to appear, and Ayato must be ready to attack. And when it does, Can Ayato win? Ayato comes out the winner!

Ayato and Quon are headed back to Tokyo Jupiter. Elvy is ordered to go out and bring them back, using the Vermillion, at any cost. Even if Ayato comes back peacefully, Iishiki plans to charge him for treason. Haruka asks to go with Elvy secretly, and she lets her. Ayato is almost to Tokyo Jupiter when Elvy catches up, and the two are about to fight when a Dolem appears to help Ayato. It distracts Elvy long enough for him to get through, then goes through too. Elvy also goes in after them. Ayato awakes in the hospital. His mom comes to get him and Quon stays there. On the way home, Ayato sees his friends and talks to them. Asahina freaks out, saying something's wrong and she's forgetting things. Mamoru tells her she's being paranoid. When Ayato gets home, he checks his blood, which is red. His mother shows him hers, which is blue. He starts to scream, and Quon wakes up.

All that Ayato has known about his life proves to be a lie: his mother is not who he thought she was, his old friends are spies and Tokyo Jupiter is infested with Mu. The only person he can trust is his old school friend, Hiroko Asahina. Together they decide to escape the city for the real world

The fight with the Dolems begins. Many human lives are lost, including Cathy and John. Ayato joins with Ixtli and the RahXephon transforms.

The RahXephon has transformed into its final state and the battle between the Xephons has begun. The outcome will not only determine the fate of Ayato and his loved ones but also the world.