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!

Watari and Kunugi are coming back to Nirai Kanai, with an Yamato Communcations reporter, Futagami. While coming to Terra is the Alpha Squad, who join with Elvy to take the place of her killed/wounded colleagues. Meanwhile, Futagami goes to Rikudo's place, to find information for Ayato. And when Alpha Squad and RahXephon attack a giant Dolem, it releases smaller dolems. And Ayato must defeat it and does.

After Celebrating New Years, it's back to the beach. Quon wanders off, and Ayato follows her. They come up to ruins located in the forest. Apparently Quon and Ayato go missing, and and Haruka starts a search to find them. Quon and Ayato are off somewhere, and Haruka's search was stopped due to the fact they were no where to be found. Haruka ends up back at the ruins, where Quon and Ayato reappear in front of her again.

B-story line: While Ayato and Quon are missing, Itsuki tries to pilot the RahXephon, but fails to do so.

A dolem is beating RahXephon, and Ayato is writhing on the floor of the cockpit, and is in a dream state where, Toyko is much different, there are flashes of a Murian, Mamoru, Hiroko, Haruka Mishima and his mother.

A photographer heads out to a mysterious archeological site, but is promptly shot to death by the very woman who brought him there. At Nirai Kanai, Sayoko and Mokoto are getting together. Haruka is shocked when she walks by and sees him leaving. Helena, of the Barbem Foundation sends Doctors to investigate Quon, who is in a deep sleep. A new Dolem attacks, and both RahXephon and the Alpha Squad is sent out, but Ayato becomes distracted when he finds Quon inside RahXephon with him...

Despite Itsuki's report saying Quon has not yet awakened, Helena has "reliable information disputing that," namely the disc that Sayoko gave to Makoto. Itsuki is mad at Sayoko for this betrayal. Futagami reveals an odd family secret.

Megu is going through a test to become a full-fledged member of TERRA. Ayato is still depressed because he's a Mulian and everyone was keeping it from him. He's going around biting people's heads off, accusing them of laughing about him behind his back. Haruka is worried about telling Ayato some secret. The two of them talk. Haruka says that it doesn't matter that Ayato is a Mulian, but he doesn't listen. Sayoko breaks it off with Iishiki, saying that he was using her, but she was also using him. She gives him a dress as a token, because she no longer has anyone to wear it for. And Quon is about to be moved to her new home. Megu passes her test and she is going to meet someone to tell him about her feelings for him. But when she goes to meet him, she finds that Souichi is already in a relationship with Kim. She's upset at first, but Kim starts to cry, so Megu forgives her. Quon asks Ayato to take her to Tokyo and he agrees, flying off in the RahXephon.

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

While on the run from the authorities, Ayato and Asahina grow closer as they start a life together and try to blend into the rest of society. Free of Tokyo Jupiter effects, though, Asahina soon discovers something about herself that frightens her. Fearing that Ayato would leave her if he knew her secret, she decides to keep the news to herself.

Ayato returns to TERRA amidst many changes: Isshiki is in charge, the mysterious Mishima is now a part of TERRA, and Mamoru has arrived from Tokyo Jupiter and is willing to live in the real world.

Ishiki plans to destroy the barrier around Tokyo Jupiter. Souichi is planning on tricking him somehow.

Ayato finds out from Itsuki that Haruka is in love with him, and is hurt that he didn't even know and he's been avoiding her.

Mamoru has been going through Ayato's stuff and has found out that he's close to Megu by listening to his cell phone message. He spends more time with her. He also finds Hiroko's diary, with the blue blood and the good-bye message. Later, he walks outside with Megumi. Ayato finds them. Mamoru grabs Megu around the neck and says that Ayato killed Hiroko, even though he knew she loved him. He says that Ayato will have to make a choice soon, and he will no longer be human. He punches Megu in the face.

Eager to prove himself, Ishiki fires Haruka over a trivial matter and takes control of the attack on Tokyo Jupiter. Against orders, he moves the attack up one hour. The attack commences with disastrous results.

Meanwhile, Ayato is busy finishing up his painting when he receives a call from Kunugi to pick up Mamoru's cat. While there, he learns how Haruka saved him from the concentration camps. Returning home, he finishes his painting. He is about to show Haruka when Mishima appears and reveals her true purpose for her existence and Ayato's destiny with the RahXephon.

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

Tensions mount as the survivors struggle to rebuild their lives among the ruins of Japan. As arguments become heated, Haruka questions her sanity as she begins to see Ayato in various places. Meanwhile, Quon prepares to make her final move.