Three years have passed since the attack of the Legion, and the world is once again plagued by Gyaos attacks. The flying monsters, thought to have been wiped out by Gamera, are now reappearing in increasing numbers across the globe and have evolved into Hyper Gyaos. Mayumi Nagamine, noted ornithologist, returns to aid the Japanese government in addressing this threat. A graveyard of Gamera fossils has been found at the bottom of the sea. Shadowy government agents Miss Asukura and Kurata Shinji, the former with occult beliefs, are meanwhile working to a different agenda, with Asukura believing Gamera to be an evil spirit.
Tragedy strikes, however, as the kaiju take their conflict to the populated Shibuya district of Tokyo. Two Gyaos glide across the city skyline, relentlessly pursued by Gamera. He manages to blast one of them with a plasma fireball over the city, sending its flaming body into a collision with a crowded subway. Gamera bursts into the station in order to finish off his foe, incincerating the dying Gyaos along with several city blocks. Gamera then pursues the second Gyaos, firing several fireballs at it until it is destroyed. Gamera then flies away into the night sky. An estimated twenty thousand human lives are lost in the battle, and the Japanese government orders Gamera's immediate destruction.
Meanwhile, a young girl named Ayana copes with the loss of her family, who were inadvertently killed by Gamera during his Tokyo battle with Super Gyaos in 1995. A maelstrom of hatred and despair, Ayana finds friendship in the oddest of places: a stone egg sealed within her village temple. The egg hatches a small tentacled creature, whom the girl names "Iris." Iris becomes the focus of Ayana's quest for revenge, as she seeks to raise her own monster and take vengeance against Gamera. Revenge comes at a price, however, as Iris attempts to absorb Ayana in the process of its growth. The girl's foster brother manages to free her from Iris' cocoon, but its taste for humanity is far from quenched. It escapes and kills half of the populace of the village. Iris then grows into his monstrous adult form. After killing a young woman, the military was called in, but failed to stop Iris.
Iris flies toward the city of Kyoto, but is intercepted in mid-flight by Gamera. The monsters engage in a high-speed battle in the night sky, Gamera using his saucer-like locomotion to slice Iris. The Japanese army intervenes, however, knocking Gamera out of the sky with a tactical missile strike. Iris then proceeds unimpeded to Kyoto, where Ayana has been taken by Asukura and Kurata, with Asukura deliberately trying to use the girl to summon Iris; Nagamine and Asagi, the girl once psychically linked with Gamera, retrieve her and attempt unsuccessfully to get her out of Kyoto. Kurata expresses a belief that Iris has been deliberately created to defeat Gamera so that the Gyaos can wipe out modern humanity.
Ayana lends her will to Iris, as Gamera dives on Kyoto and fires several fireballs towards Iris. Iris easily bats them away with his tentacles, and the city erupts in flame. The two monsters engage in melee, but Iris easily gains the upper hand, impaling his foe and leaving Gamera for dead. Iris then makes his way to the train station, killing Asukura and Kurata and opening his chest to finally absorb Ayana.
From within Iris' body, Ayana experiences the creature's memories, and realises that her hatred and bitterness motivated him. Just as she has her epiphany, Gamera smashes into the station and plunges his hand deep into Iris' chest. Gamera manages to wrench the girl free, robbing Iris of its human merge, but it counters this by staking Gamera's hand to the wall with one of his dagger-like arms. Miss Nagamine and Asagi, trapped within the train station's wreckage, watch helplessly as Iris begins to syphon Gamera's blood, and create fireballs with its tentacles. Before they can be launched, however, Gamera takes action, choosing to instead blast off his own impaled hand. Iris launches the fireballs, but Gamera absorbs the blast into his stump, and forms a fiery plasma fist, and drives it into Iris' wounded chest.
Iris explodes, blowing the roof off the crumbling train station. The comatose Ayana still clutched in his fist, Gamera sets the girl down where Nagamine and Asagi are hiding. The women are unable to revive her, but Gamera lets out a roar and Ayana opens her eyes. Gamera leaves the girl wondering why he would save her life after all she had done, and the three survivors watch as the Guardian of the Universe marches into the fire-streaked night. The swarm of Gyaos, thousands strong, begin to descend on Japan intent on destroying their greatest foe once and for all, as Gamera lets out a final roar of defiance.
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