The city of Tokyo has been overthrown, taken over by the Mu, invaders who have devastated the rest of the planet. Within the domed walls of the city, however, time flows in a different path, and none of the citizens even know they've been conquered. An extraordinary mystery unfolds as Ayato confronts a world he has never known, and begins to learn the horrifying secrets of RahXephon, a humanoid super weapon which apparently only he can control.
Life for Ayato Kamina seems normal enough, but when wars hits close to home, the life he once knew changes forever. As if guided by fate, Ayato has chance encounters with Haruka, a woman trying to protect him from mysterious government agents and Reika, a friend who guides him to the secret Shrine of Xephon. It is there that he wakens the powerful force that will alter everything that he once knew.
With the RahXephon awakens, the tide of war seems as if it is about to change, The RahXephon, under the control of Ayato, easily eliminates the invading Dolem, showing its vast capabilities and power. After the battle however, it seems that what he thought he saw didn't really happen. Someone is hiding the truth, whatever that may be, but Haruka offers to show him the reality of the situation.
Ayato has discovered the shocking truth: his mother has blue blood, and nothing is as it seems. The RahXephon destroys another Dolem and creates a passage from Tokyo to the outside, where Haruka has more startling revelations for him. Tokyo has been under the control of the Mu for quite a while, and it is sealed in a huge protective membrane. With no way to return, Ayato tries to cope with the levity of the situation.
Having left the "safety" of Tokyo and now living on the outside, Ayato and Haruka are picked up by TERRA, the military group that she belongs to. They depart the Mu infested Tokyo for safer ground. Commander Kunugi fears that despite his red blood, Ayato may still pose a threat, especially with the traces of Mu blood found in his system, and the RahXephon is to be transported elsewhere for further study.
Having taken care of the Dolem threat, Ayato has proven that he can be trusted, and is taken to a new home. The RahXephon though is showing signs of petrifaction, and the thought is that since it has synchronized itself with Ayato, this has to do with his feelings towards the TERRA members.
The media has somehow picked up on the knowledge that TERRA has a new weapon in their fight against the Mu, but they keep running into a brick wall of plausible denial. Kim has memories of tragic events that have a great deal to do with her joining TERRA, and despite his reluctance, Ayato once again pilots the RahXephon against an invading Dolem.
A man calling himself an "observer", Makoto Isshiki, is brought in to join with TERRA, but his true purpose seems rather questionable. Additionally, a reporter is brought in to attempt to bring in some good public relations for the organization.
A crystal that Kisaragi has given to Sayoko has some adverse effects, and it's not just on her either. The temperature on Nari Kanai changes from tropical to winter like conditions, to take make matters worse, the crystal possesses Sayoko and she soon finds herself as part of another Dolem. Ayato must make the choice between destroying the enemy or saving Sayoko.
What starts as a typical day at the beach turns into a mystery. Ayato sees a woman that he believes to be Reika, and he and Quon go to investigate. The two stumble upon a peculiar and ancient construct that they proceed to investigate. However, the two disappear without a trace, and what seems like merely minutes to them is in fact days to those on the outside.
Itsuki has been experimenting with music to grow plants, and a piece of music that Quon has been playing recently has had a rather strange effect on them, especially when their original and shabby state is taken into consideration. But, the piece of sullen music seems to serve another purpose to someone else at TERRA.
During a recent encounter with a new Dolem, Ayato's life support systems fail, and it seems that he may have finally met his end. However, he finds himself once again back in Tokyo Jupiter in the life that he once of, or at the very least, thought he did. And while the team at TERRA struggles to get him to respond, he himself must find the inner strength to pull himself out of this bizarre waking dream.
Quon has fallen into a strange catatonic state and is hospitalized. To everyone's surprise, she suddenly vanishes, and the search is on to find out just where she went. However, it seems that her "coma" is a prelude to something bigger, an awakening of sorts.
The question on everyone's mind is "Who is Quon?" Itsuki claims that she is his sister, but other information surfaces that indicates otherwise. Meanwhile, the latest toy from Bahbem, a new mecha called the Vermillion is tested on and off the battlefield.
A shake up at the base takes place when the corporate interests use their influence to take charge of Quon. A new Terra weapon, The Vermillion, debuts. The pilot, Elvy, and her crew make it clear that they no longer want the RahXephon around since they don't trust his heritage and no longer need him.
The present becomes the past as the focus shifts to the Bahbem Foundation. Three young children, Itsuki, Helena, and Isshiki, live there as students; Isshiki finds a Dolem living in the ruins beneath the mansion and wants to protect it. However, his desire to save what he believes to be a living creature will be nothing more than a bitter dream.
Still searching for the truth about what he is, Ayato toys with the idea of returning to Tokyo Jupiter. However, his trip may come sooner than he planned.
TERRA sends Elvy to catch Ayato and Quon, as well as bring back the RahXephon, their best defense against the Mulian invasion. Though returning to Tokyo Jupiter may have seemed like a fantastic idea, Ayato quickly learns that much has changed, including many of the more simple things in his former life.
Ayato's life is falling apart. His mother isn`t who she seems to be, his friends seem to have been sent to spy on him, and Tokyo Jupiter has an even greater Mu presence than when he left. It seems that his only salvation is with Hiroko, and together the two decide to leave the Mu infested Tokyo and return to the safety of the real world.
Now that he's left Tokyo Jupiter, Ayato seems to only have one person he can rely on, and that's himself. He can't return to TERRA, and he and Hiroko try and simply blend in with the rest of the world. However, little do the two know that TERRA already knows he's back, and they are looking for him.
Ayato is back with TERRA again, but now Isshiki is in charge, and that`s not good for anyone. Mishima has suddenly appeared as well, and it seems that she is now a member of TERRA. Mamoru has arrived from Tokyo Jupiter, and it seems as though he`s ready to accept what lies beyond the only world that he knew.
Tempers and attitude flare as Isshiki`s take-over of TERRA begins to take its toll. Mamoru finally learns what happened to Hiroko when she came over with Ayato, and he reveals the truth as to why he has come. Isshiki also reveals his plan to take down the barrier around Tokyo for good.
Ayato has a face-to-face encounter with Mishima who reveals her true purpose for showing herself. Ayato however doesn`t believe her. Isshiki and TERRA initiate their plan to take down the Tokyo Jupiter barrier, but the results endanger the world, and we finally see the deceptive man get what`s coming to him.
The Mulian forces have issued an ultimatum: hand over the RahXephon or face annihilation. However, TERRA decides against this course of action, and although it seems the deck is stacked against them, they choose to fight.
As the battle rages on between TERRA`s forces and the Mulian invaders, Ayato finds himself in a position where he must finally choose which path it is that he will inevitably take. Meanwhile, some of the key players begin to reveal their true purpose.
With Japan in ruins, the survivors begin to pick up the pieces of their shattered lives and try and slowly rebuild. The now evolved Ayato appears, and Quon makes her final move.
It's the final battle between the two True Xephons, but there will only be one winner. It is clear that is has all been orchestrated for a higher purpose, but why still remains a mystery.