Two years ago, Jin Kamishina survives a shuttle accident which killed the rest of his family. Now eighteen years of age, Jin lives a solitary existence, often avoiding questions about the rumors of the shuttle pilot (who was his dad) error. Meanwhile, Earth faces possible destruction from an asteroid, so the ISDA works on the "D-Project". In a facility, Kazuki Tachibana, Jin's old friend, is being tested for his compatibility with a dragon, which is a success. Elsewhere, Jin witnesses a strange creature kill a woman. The creature then goes after him too, and eventually catches up to him, causing Jin to fall out the window. However, Jin is caught by a mysterious girl who is able to fight off the monster. When Jin wakes up, the girl introduces herself as Toa.

Jin suddenly wakes up in an ISDA room, where he is questioned about the shuttle accident two years ago. He is also told the truth about the asteroid Thanatos, in which extraterrestrial life called Dragons came to Earth from Thanatos. Hearing that one of these dragons was the cause of the shuttle accident, he asks them to tell the truth to the public, so his father's name could be cleared. They deny his request and instead ask him to become a Dragonaut, which he rejects. He then meets Kazuki Tachibana, his old friend, who now works for the ISDA. Later, Jin remembers where Toa is to meet him, so he runs away from the ISDA to see her. The two are finally reunited, but it is cut short when the ISDA attempts to capture Toa. During their attempt, one of their own, Spirytus, transforms into a dragon and attacks Jin. In order to protect Jin, Toa reveals that she too can transform into a dragon.

Toa and Spirytus continue their battle as dragons, but once their battle reaches a critical point, the ISDA is given permission to interfere in the battle. Thus, Machina, Amadeus, and Howlingstar transform into dragons, controlled by their "pilots", Akira, Sieglinde, and Raina, respectively. Despite the odds, Toa manages to hold her own, which is when Gio, Kazuki's dragon, arrives on the scene, having previously been awakened by one of Toa's shock waves during the battle. As Gio, who is concerned about Toa, transforms into a dragon, Jin hops on his back so he can try to help Toa. As the two reaches Toa, Jin sees a vision where Toa tells him that she can no longer be with him now that he has seen her real form. Gio then shows up to tell Toa that he was created in order to protect her, and as the two were about to link hands, Howlingstar attacks them, returning them to battle. Then, Toa accidentally knocks Howlingstar onto Gio, plunging Gio and Jin into the ocean.

During an ISDA meeting, the subject of whether or not the D-Project should be made public is brought up. Meanwhile, after Jin wakes up on a beach with Gio, they discuss what Toa is to them. Jin then hears Toa singing, which he realizes is coming from the moon. Later, Machina and Akira come across Gio who is apprehending Jin, so they bring the two back to the ISDA. As Jin is being questioned by Akira, Gio explains his actions to Sakaki, the Dragonauts' military commander. When Gio is being escorted to Yuuri, he escapes, and Jin is also revealed to have escaped after being questioned. This is when Akira realizes that Jin and Gio planned their capture; in order to get a pod necessary for Jin to go into space with Gio. After Gio's brief scuffle with Machina, Akira's dragon, Gio transforms and Jin attaches the pod to Gio's neck. They then fly off towards the moon in hopes of finding Toa.

A flashback sequence shows how the military tried a Resonance program five years ago, but it ended in failure. Presently, during their ongoing search for Toa, Gio decides to abandon Jin believing that he was wrong about Toa being on the moon, not realizing that they have just missed her. Meanwhile, back on Earth, the ISDA publicly reveals the truth about the D-Project and Thanatos. The Dragonaut team is then ordered to focus on the D-Project, whilst the military handles the recapture of Gio. In the lunar city, Jin is captured by Garnet and the military. In order to lure Gio in, Garnet sends a public broadcast about Jin's capture, but in a frequency which only dragons can hear. Gio initially ignores the broadcast, but after accidentally seeing Toa in a video that some kids took, he goes to save him. During his attempt, Gio battles Garnet while being weakened by a machine, but as Jin tries to escape, he destroys the machine. Gio then saves Jin and transforms into a dragon.

During a flashback, it is revealed that Jin had been operated on after the shuttle accident, during which Yuuri, an ISDA researcher, claims to have noticed signs of a Resonance. In present time, Yuuri and Sakaki request for Kiril to reassign the Lindworm Unit to capturing the Album [Toa]. The mission is accepted so Raina, Akira, and Sieglinde travel to the Moon, where Jin and Gio continue their search for Toa. As Yuuri arrives home, she unexpectedly encounters Kō, who shows her incriminating evidence regarding Amagi. Back at the moon, in a coffee shop where Toa had been staying, she is encouraged by the owner to not deny her feelings, so she decides to go look for Jin. When she finally finds Jin and Gio, Howlingstar, Amadeus, and Machina arrive in order to capture her. Gio interferes and fights Howlingstar, and as Amadeus takes Jin to Sieglinde, Machina engages Toa, but instead of fighting, she asks Toa why they were born, to which Toa replied that it is all due to destiny.

After finally reuniting, Jin, Gio, and Toa receive tickets for a spa resort from the coffee shop owner. At the spa, Jin and Toa deepen their relationship, while Gio continues to wonder about his purpose and his own relationship with Toa. Unbeknownst to them, the Lindworm Unit, with the exception of Raina, who is secretly meeting with Garnet, also takes a break at the spa resort. After being spotted, the two groups engage in a battle that breaks the pool's floor, resulting in their separation through underground waterways. Jin and Sieglinde end up with each other, so though some complications arise, past memories allow Sieglinde to soften up to Jin. The two are later found by Gio, who was working with the others in order to find Toa. As both groups reunite, Jin, Toa, and Gio fly off, with Sieglinde allowing them to escape. Meanwhile, back on Earth, Kazuki once again meets the woman, Widow, whom he had met earlier.

After escaping from the spa resort, Jin, Toa, and Gio try to figure out what to do. Jin believes that the three of them can just live peacefully in some small town back on Earth. Despite Toa's desire to do so, she has a "mission" to fulfill, so she abandons Jin and Gio while they are sleep. Once Jin wakes up and realizes that Toa is gone, he tries to look for her, but is thwarted when Kazuki and Widow show up. Kazuki demands Gio back, but Jin is more concerned with looking for Toa. After Gio frees himself from Widow's clutches, he picks up Jin and runs off. Meanwhile, Toa surrenders herself to Raina, who had just been in a meeting with Kō. Still desperate to get Gio back, Kazuki offers to help Jin get Toa back if Jin agrees to give him Gio. His hesitation prompts Kazuki to send Widow to retrieve Toa. When Jin tries to apologize to Gio, Gio asks if Jin can protect Toa, and after hearing that Jin can, Gio realizes that he has been getting between Toa and Jin all along.

It is revealed that when the shuttle exploded two years ago, Sakaki's wife and daughter had been on board. In present time, just when Jin hears Toa tell him that she was responsible for his family's death, the Lindworm Unit suddenly appears to ambush the trio: Jin, Gio, and Toa. Meanwhile, as Garnet and the military look over the Resonance data they received from Raina in exchange for giving up their search for Gio, they realize that it is fake. In retaliation, she later attacks the shuttle carrying the trio. When Gillard Army begin to corner the Dragonauts, they are saved by a fourth dragon from the Vritra Unit, but the Gillard military ships continue their attack. As enemies board the shuttle containing the trio, Gio makes Jin, who has been focused on Toa's confession, remember his promise to protect Toa. Gio then actualizes with Jin as his pilot. They quickly destroy most of the enemy's forces, causing Garnet to retreat.

During an ISDA meeting, Kazuki's actions as a Dragonaut, and the current situations of the Album, Jin, Gio, and Widow are discussed. Meanwhile, Gio and Widow are confined in a facility that prevents them from leaving. At the ISDA base, Yuuri explains the Resonance process to Jin, and tells him that he had resonated with Toa two years ago. Elsewhere, Garnet is trying to apologize for her failures to Prince Asim, but he is now more interested in obtaining Toa rather than Gio. Back at the ISDA, Toa breaks free and attempts to retrieve some dragon eggs, but Kasuga's glowing eyes make her hesitate, giving Amadeus a chance to knock her unconscious. Using the confusion caused by Toa's attempt to escape, Akira and Machina free Jin. Laina and Howlingstar attempt to stop them, but after Machina uses Laina as a hostage, they end up successfully escaping. Later, when the ISDA decide to transport Toa, they are attacked by the Gillard military.

After escaping, Jin, Akira, and Machina realize that they are not being followed by the Lindworm Unit, so they take refuge in an abandoned house. Meanwhile, Toa has been captured by the Gillard military. Yuuri, who was left behind by Nanami, swims to Tartarus in order to contact the ISDA and inform them of Toa's capture. On board a space station, the ISDA's Vritra Unit is having a briefing on the missile that they plan to use against Thanatos. Toa meanwhile has been delivered to Prince Asim on Mars, but when she attempts to tell him the consequences for capturing her, he ignores her, being more interested in seeing her true form. Later, a fourth dragon from Thanatos appears near Earth, and destroys the Vritra Unit, except for Itsuki and Otohime, who both manage to survive. The dragon then enters Earth's atmosphere, where Machina appears to recognize it.

The original fourth dragon, which the ISDA name "Ostrum", wreaks havoc on Earth and then suddenly disappears before the ISDA can take action. Kasuga informs the ISDA that Ostrum has resonated with someone, but he does not know who. Ostrum later reappears, and enters into battle with the Lindworm Unit, but Ostrum overpowers them. Akira, who's watching from afar, decides to help her comrades, and joins in the battle with Machina. Meanwhile, Jin is helped by Kō, who takes him to Tartarus. Upon their arrival, Jin is obstructed by Kazuki, who still claims that Gio belongs to him. Back at the ISDA base, Kasuga is confronted by Yuuri. After refusing to answer her questions, he proceeds to have the computer drop the container holding the ISDA's original dragon sample. Ostrum, who had succeeded in losing the Lindworm Unit, appears in his Communicator form, and asks Kasuga why he decided to side with humans. Back on Tartarus, Gio is able to transform into his dragon form and flies off with Jin.

A flashback sequence from ten years ago reveals the origin of the development of the D-Project. In the present, Ostrum continues to do battle with Atrum, and after they both return to their Communicator forms, Kasuga tries to explain why he is protecting humans. Meanwhile on Mars, Toa tries to get Asim to allow her to change into her original form so she can escape, but fails to do so. Back on Earth, Otsolm and Kasuga battle in their Communicator forms, but when Ostrum senses another dragon [Gio], he leaves in order to dispose of him. On Mars, Nanami decides to free Toa in order to get her to save Earth, but is subsequently shot in the back by Garnet, who once again confines Toa. Figuring out Toa is on Mars, Jin and Gio head towards space, but after the Lindworm and Vritra Units fail to destroy Ostrum with the Type-X warhead, they return to finish the job using the warhead.

In a flashback, it is shown that Raina had known Jin's father. Back in the present, Raina and Howlingstar check up on Jin and Gio. Raina offers Jin to be a Dragonaut, but Jin does not believe he deserves to be one. Meanwhile, Kasuga explains his origins and reasons to Yuuri. At another location, Akira talks to Sieglinde, but is interrupted by an ISDA broadcast. Later, Jin and a revived Gio team up with Akira and Machina, and proceed to head into space toward Mars. However, before they can leave Earth, a deranged Kazuki attacks Gio on board Widow, inflicting damage to ISDA structures in the process. Their battle results in Kazuki and Widow being engulfed in an explosion. Jin, Gio, Akira, and Machina then continue to head into space. Meanwhile on Thanatos, a creature awakens.

A flashback of 15 years ago reveal that a young Asim had encountered a dragon egg which had resonated with him. Back in the present, Garnet releases her true powers and stabs Gio in the stomach. Gio still manages to escape with the others, and ends up in an abandoned facility, where Toa heals Gio's wound. The group then stumbles upon an underground hot spring. There, Gio and Jin bond further, while the women talk about Toa's "stigmata", which signifies a dragon's impending death. Later, Akira performs a wedding-like ceremony for Jin an Toa, but the group is subsequently interrupted by Asim. When Garnet lunges to attack, Akira jumps in her way, and receives a fatal blow. Akira's death causes Machina to go berserk.

A flashback of how Asim gained his title twelve years ago is shown. Back in the present, Asim and Toa argue about the nature of the human race. Just when Toa talks about the power love can create, Asim informs her of Jin's arrival. Jin and Gio head toward Toa's location, as Akira and Machina stay behind to fight off Mar's fleet. Gio, in his Communicator form, and Jin storms the main building, and eventually arrives in the throne room. Gio is confronted by Garnet while Jin is attacked by Asim. Toa, witnessing this, cries out, resulting in the glass, which surrounds her, to crack. Toa distracts Asim, allowing Jin to punch him, which then distracts Garnet, allowing Gio to knock her out. Toa and Jin embrace as they are reunited once again.

When Machina goes berserk, the other members of the Lindworm Unit sense her situation and decide to head to Mars. On Mars, Kō tells the Gillard King to remove Asim from his duties as military commander. Meanwhile, Garnet transforms into a dragon, and knocks out Machina with her tail. Gio, with Toa and Jin in a pod attached to him, easily defeats Asim's military fleet. As Gio and Garnet do battle, Machina appears in her dragon form, but is blown away by Garnet. After Gio is hit by an attack meant for Toa, he releases an incredible amount of power, engulfing both Asim and Garnet in the explosion. Jin and Toa are flown to safety by Howlingstar, who had just gotten there. In the final scene, Machina encases herself and Akira in ice.

One year later, with the ISDA under Gillard management, the Dragonauts are divided and hunted down. Since the Gillard King and Sakaki are convinced that dragons are dangerous, they are hunting down both original and artificially-made dragons, save those that are under their command. Also, there is now a new D-Project. Meanwhile, Jin, Gio, and Toa, have been living normal lives in an isolated town for the past year. Sieglinde and Kō unexpectedly show up on their doorstep to discuss the ISDA's current standpoint, and Toa tells them that Thanatos would merely leave Earth alone if it gets back its dragon eggs. Later, when Toa reaffirms her feelings for Jin, she, along with every other dragon on Earth, senses something from Thanatos.

Jin, Toa, and Gio's house is burned down by Agathions sent by the ISDA as Kō takes the trio to the Baumgard family's estate, where Sieglinde's father, Wilhelm, agrees to shelter them. Meanwhile, the ISDA continues their experimentations on dragons in order to figure out the best way to destroy Thanatos, while Laura, Sakaki's dragon counterpart, captures Itsuki and Otohime. Later, the ISDA realizes that their experimentations on artificial dragons caused them to develop an immunity to the "anti-Thanatos factor", however, it may still work on original dragons. Back at the Baumgard estate, as the group heads out, Whilhelm offers Sieglinde to stay with him, but she decides that she has somewhere else where she belongs, leaving with the others.

As Jin and his comrades travel, Gio disappears without telling the others after he senses something from Thanatos. Once they reach the ocean, Jin and company encounter a submarine piloted by Yuuri and Kasuga, who invites them to board. They plan an attack on Tartarus, and as Jin and Toa battle Kazuki and Widow, the others infiltrate the ISDA base, where they find Raina and Itsuki. Kasuga realizes that Sakaki intends to use the "Aegis" on the captured dragons. Laura then appears, prompting Kasuga to fight her alone, as Sieglinde finds a way to free the captured dragons, reuniting with Amadeus. While Howlingstar and Otohime help Jin and Toa, the others check up on Kasuga. As Laura escapes upon seeing the others, she senses something approaching. Gio appears and surprises all by attacking his comrades.

Gio continues to attack his former comrades by knocking them all out. While Toa is unconscious, Gio tells Jin that he cannot protect Toa, and informs him her impending death. When Toa awakes, she refuses Gio's offer to come with him, but he then tells them that he has become Thanatos's successor. Laura then appears and attacks Gio, but is subsequently knocked out. After Gio takes his leave when Toa refuses his offer again, Toa heals Laura, who is actually the final original dragon from Thanatos, while Sakaki and Jin talk. Later, as Sakaki sees to Laura's health at a facility, they are attacked by soldiers, leading them to run away. Meanwhile, Toa and Jin reunite with their comrades, and tries to figure out their next move.

As Sieglinde and her comrades camp out in an abandoned building on an island, they stumble upon Sakaki, who has washed up on shore. Meanwhile, the ISDA conducts experiments on Laura, as Kazuki and Widow discuss her situation. At another location, Kasuga tells Yuuri about the purpose of the original dragons sent to Thanatos. Back on the island, Jin and the others question Sakaki about his motives. Gio later appears to attack Kasuga's location, but Jin's group comes to their rescue, though is incapable of dealing any sufficient damage. Just as Jin confronts Gio, Kazuki and Widow show up, but Widow is subsequently damaged by Gio after she attempts to blast Toa. As Thanatos is shown to be close at hand, Machina and Akira are shown to disappear from their ice tomb.

Gio once again advises Jin to let Toa go, then he heads toward Thanatos, which the Gillard fleet engages into battle with, though subsequently loses. As Jin and Toa spend time together, and as the others think of heading into space, Gio converses with Machina and Akira, who have merged with Thanatos as part of its soul. Later, after Jin finally allows Gio to take Toa, he runs into Kazuki, who is distraught over Widow's recent death. They have a short altercation, and end up reconciling. They later storm the ISDA, aided by Sakaki, who gets shot in the back as he sends off Jin and Kazuki in a shuttle. Laura protects Sakaki from further harm, and as Sakaki loses consciousness whilst embracing Laura, Kasuga absorbs the anti-Thanatos factor from the two.

After Sieglinde and Raina use the Aegis system to fire a beam towards Thanatos, the entire Dragonaut team, including Jin and Kazuki, are transported into Thanatos, where Akira and Machina greets them. The two explain Thanatos' true nature and its intentions. In disagreement, the Dragonaut team decides to leave, except Jin, who is led to Toa by Gio. Gio then tries to kill Jin in order for the latter to become one with Thanatos as well be with Toa forever, but Jin avoids his attacks and tries to talk some sense into him. Just as Toa begins to fuse with Thanatos, her love for Jin suddenly reunites them. Intrigued by this, Thanatos, in the form of Garnet and Asim, decide that instead of destroying humanity, it will fuse with it. Jin, Toa, and Gio then leaves Thanatos as it prepares to assimilate with all of humanity.

Members of the Dragonaut team attempt to protect as many humans as they can from the billions of Ostrums sent by Thanatos. Meanwhile, Toa, Jin, and Gio try to approach Thanatos since Jin wants to persuade it to stop. Kasuga helps them get through by blowing himself up, taking out massive amounts of dragons in the group's way. Once inside, they are met with the original Ostrum, whom Gio decides to battle himself while Jin and Toa go on ahead. Jin and Toa then encounter Garnet, who sends Jin into a dream world where the shuttle accident never happened, however, Jin is able to snap out of it by following Toa's voice. As Gio is able to defeat Ostrum, the power of Toa and Jin's love for each other results in the deactivation of all the Ostrums, the disappearance of Toa's stigmata, and the appearance of "mother", who decides that she will think about the meaning of love as she moves on to the next planet. In the end, Gio leaves for space, and Jin and Toa are able to live on together.