One year after the battle between Gamera and the Gyaos, a bright meteor crashes in Hokkaido, setting off a chain of alarming discoveries. The Japan Ground Self-Defense Force (JGSDF), led by Colonel Yusuke Watarase, rushes to the impact site, unaware that insect-like extraterrestrials have begun to emerge from the fractured space rock. Meanwhile, a string of telecommunication failures draws the attention of NTT engineers, who uncover that underground lines in the affected area have been entirely ripped away. The network is not just down—it seems to trace a deliberate path south from the crash, a clue that something nonhuman is moving beneath the surface.
At the heart of the technical scramble is Obitsu, a diligent network engineer who notices that the missing cables form a straight line leading away from the site. Soon, the alien presence makes itself felt in Sapporo, where the creatures march toward the city and bore into the subway, establishing a hive within the tunnel labyrinth. When Colonel Yusuke Watarase and a contingent of JGSDF soldiers descend into the dark tunnels, a pod-like structure rises from the ground and begins to alter the air—its rapid increase in oxygen signals a purpose beyond mere invasion.
The trio of human minds—Watarase, Obitsu, and Midori Honami, a science instructor—put the pieces together: the pod is a biological launch pad intended to eject a seed into space to colonize another planet, and the heightened oxygen would fuel a spectacular, devastating launch. Destroying the pod would be catastrophic for Sapporo itself, so they face a grim dilemma: defend the city or risk annihilation if the seed fires. As the tension climbs, Gamera resurfaces from the sea to intervene, tearing the pod loose but finding himself swarmed by the invading insects and driven back to the depths.
In the wake of Gamera’s withdrawal, a larger creature surfaces underground, spurring a second hive to form. A soldier named First Lieutenant Hanatani dubs this emergent swarm the “Legion,” a name that will echo through the coming battles. The Legion turns its sights on Sendai, prompting Watarase to order the evacuation of the city. Midori Honami teams up with Asagi Kusanagi, a teenage girl who shares a remarkable psychic bond with Gamera, and the two become a focal point for the city’s hope. As Honami’s helicopter crew attempts to evacuate, Asagi Asagi Kusanagi is drawn into the psychic link, guiding Gamera toward a crucial confrontation.
A tense aerial encounter unfolds as the Legion Queen and Gamera clash above Sendai. The Queen lands a brutal blow, severely injuring Gamera and sending him retreating underground as Honami and Asagi slip away to safety. Back on the ground, Watarase’s forces race to evacuate the city, while the scientists deduce that the Legion are silicon-based creatures drawn to electromagnetic sources. The threat is escalating: two hive attempts have already failed, and the Legion heads for Tokyo with little resistance, assuming Gamera is dead.
Desperate to save humanity, Honami returns to the ruins of Sendai Station to seek a way to revive Gamera. Asagi reaches out in the psychic connection, and for a moment Gamera stirs from dormancy, though the bond is severed when Asagi’s protective amulet shatters. The Japanese prime minister orders a nationwide mobilization of the JSDF to halt the Legion before it reaches Tokyo, and a final, coordinated defense is mounted.
In the climactic showdown, Gamera engages the Legion Queen with the support of the defense forces, while Obitsu and Watarase implement a trap at a nearby power plant to thin the swarm. Gamera tears the queen’s horns away, seemingly gaining the upper hand. But the queen returns with a renewed assault, unleashing laser-whip attacks that shred at Gamera’s defenses. In a defining moment, the hero draws upon the collective mana of humans around the world, unleashing a plasma cannon that opens in his chest. The barrage shatters the Queen, ripping her apart and signaling the apparent end of the Legion threat. As the dust settles, Gamera soars skyward, and Asagi’s tearful farewell marks a poignant close to the battle for humanity’s fate.
