A ship carrying plutonium collides with a floating atoll off the eastern coast of the Philippines, one of many incidents occurring throughout the area. As the anomalous formation approaches Japan, a team of scientists led by Naoya Kusanagi (Akira Onodera) discover orihalcum amulets and a stone slab covered in Etrurian runes on the atoll. During the investigation, the atoll suddenly quakes, destroying the slab and throwing the scientists into the ocean. One member of the team, Marine Officer Yoshinari Yonemori (Tsuyoshi Ihara), sees the eye and tusk of a giant turtle.
Three years have passed since Gamera defeated the Legion, and the world is once again plagued by the Gyaos, which have evolved into Hyper Gyaos. Mayumi Nagamine, noted ornithologist, returns to aid the Japanese government in addressing this threat. A graveyard of Gamera fossils is found at the bottom of the sea. Shadowy government agents, occultist Miss Asukura and Kurata Shinji, are meanwhile working to a different agenda, with Asukura believing Gamera to be an evil spirit.
A year has passed since the battle between Gamera and the Gyaos, and Japan has struggled to rebuild its cities in the meantime. The military has kept a cautious vigil on the nation's coast, but so far Gamera has yet to return. Suddenly, a series of bizarre incidents reveal a new threat to the land of the rising sun. On a moonlit stroll, science instructor Midori Honami watches as a huge meteor plunges into the mountain snow. The next night, two security guards are horrified as they see large insect-like creatures stealing glass bottles from a nearby warehouse. Soon after, the entire city of Sapporo is covered with strange plants and the link between these events soon becomes clear.
Gamera self-destructed to destroy several Gyaos in 1973, the tale picks up thirty three years later, when the son of one of the survivors of that incident finds an unusual egg, from which a baby turtle hatches. The boy, Toru, raises the creature, quickly realizing it as remarkable in that it hovers and breathes fire. The creature quickly outgrows the house, is relocated by Toru and his friends to maintain secrecy, and then disappears.
In an icy North American region, an unknown aircraft is shot down by an American fighter jet. The aircraft crashes and its cargo, a low-level atomic bomb, explodes. The resulting cataclysm awakens a giant, prehistoric monster called "Gamera", who has the appearance of a giant turtle with large tusks. Japanese scientists on an expedition (including Dr. Hidaka, Kyoko, and Aoyagi) nearby are given a "devil stone" by an Eskimo chieftain, who explains that the creature is called Gamera.
Set after the events of Gamera, a meteorite collides with the rocket transporting the creature to Mars. Now free, Gamera returns to Earth and destroys Kurobe Dam in Japan. At the same time three mercenaries are sent by Kano, a WWII veteran, to an island in the South Pacific to retrieve a huge opal he once found and hid in a cave. Despite warnings from the local villagers, the trio find and locate the opal, but one dies from a fatal scorpion sting. The second man, Keisuke, Kano's younger brother, is betrayed by his fellow expeditioner Onodera and apparently killed in a cave-in.
A series of volcanoes erupt in Japan. The eruption at Mt. Futago (in Shizuoka Prefecture) attracts Gamera, whose arrival is witnessed by a young boy named Eiichi. Gamera then climbs up and into the volcano. A research team is dispatched to the volcano to find Gamera and study the effects of the eruption. Meanwhile, Chuo Expressway Corporation is building a roadway nearby, but local villagers refuse to leave.
A deadly alien force approaches Earth. Gamera intervenes and destroys the alien vessel; but before the ship is destroyed, the aliens broadcast a warning to their world stating Gamera is their enemy.
While scanning the skies through their telescope, two young boys, Akio and Tom, spy a spaceship descending into a nearby field. Stunned, bewildered, and bemused, they tell Akio's mother what they have seen, but she dismisses their story as childish nonsense. The next day, the two boys—with Akio's younger sister, Tomoko, in tow—bicycle to the site to investigate. Enthralled, Akio and Tom manage to steal into the spaceship. But then, without warning, the ship takes off, leaving Tomoko behind. It soars into outer space toward a field of asteroids, which sends the boys into panic. However, Gamera (obviously aware of the boys' plight) appears and clears a path for the ship through the asteroids. The spaceship, flying near the speed of light, leaves Gamera behind and transports the boys to an unknown planet, where it lands on the outskirts of an alien city. Suddenly, a silver "Space" Gyaos appears, menacing the ship and the two young boys. Just before the creature attacks, a second, bizarre monster—whose head resembles a ginzu knife—emerges from an underground lair and attacks the Space Gyaos. The Gyaos emits a beam that reflects off the new creature's blade-shaped head and cuts off its own leg. After a short battle, the knife-headed creature lunges and chops off one, then the other, of the Gyaos' wings. The creature cuts the helpless Gyaos' head off and brutally cuts the body into smaller pieces and then retreats back to its lair.
In Gamera vs. Jiger, Gamera has his hands full right from the very beginning. Japan is preparing for the 1970 World's Fair, to be held in Osaka. Construction of the various buildings and pavilions is well under way. On Wester Island in the Pacific Ocean, a large statue of mysterious origin (called the Devil's Whistle) is located by scientists. Workers from the Expo are interested in returning the statue for display, and try to remove it for transport by ship. The removal of the statue is hampered first by a tribal member of the Wester Island people, then by the unexpected arrival of Gamera, who aggressively attempts to prevent the removal of the statue, only to be shot at by the crew instead. The statue is removed from the island successfully after a volcano erupts. Shortly after departing the island, members of the ship's crew begin to fall ill. The statue appears to be the source of the outbreak, as it makes a continuous piercing sound, driving many of the crew members insane. Later analysis reveals the presence of a central shaft that runs nearly the length of the statue top-to-bottom. The position of the opening on the statue is creating the high-pitched 'squeal', as air passes through it.
Without warning, an alien spaceship attacks a Japanese moon base. Back on Earth, young Kenichi Ishikawa; his father, Dr. Yosuke Ishikawa; his friend Helen; and her father, Dr. Tom Wallace, witness the spaceship descending into the ocean. They go to investigate but are soon captured by a teleportation beam that brings them aboard the spaceship. Inside the spaceship, a human-looking woman appears to them and reveals that she is of a race called Zigra. By way of demonstrating Zigran technological prowess, she creates a gigantic earthquake that wreaks havoc in Japan. She previously caused two other earthquakes, one in Peru and the other in Arabia. She then tells her prisoners of Zigra's history and its great scientific advances—which, unfortunately, have resulted in the destruction of the planet; but in searching for a new home, Zigra has found Earth. The woman contacts authorities on Earth and orders them to surrender or she will kill her prisoners. Tom declares that the Zigran woman is insane, and, in anger, she sends the two men into a hypnotic trance. Kenny and Helen take action, successfully using the ship's control console to escape. Enraged, the Zigran overlord—a strange, shark-like being—orders the woman to go to Earth and kill the children. She says it would be simpler to kill all the people of Japan, but the great Zigra tells her that humans must be preserved so they can be used for food. Now, Gamera, intent on discovering the identity of the alien interloper, flies in to save the day and rescues the children and their fathers. The UN authorities, after questioning Kenichi and Helen, resolve to attack Zigra. The Defense Force jets scramble, but the Zigran spaceship makes short work of them with its powerful lasers. The alien woman, disguised as a normal human, arrives on earth and begins her search for Kenny and Helen. She hitches a ride with the Sea World dolphin trainer back to the facility, which the military is now using as its center of operations. She finds the two children, but before she can catch them, they call out for Gamera, who obediently appears.
When the evil alien Zanon comes to enslave earth, all hope seems lost. The Earth's resident superheroes, the Spacewomen, are powerless to stop him. They must enlist the help of a young boy who has a special connection with the giant turtle Gamera. The Friend of All Children then battles Gyaos (a huge flying vampiric bat/pterosaur), Zigra (an alien shark), Viras (a space squid), Jiger (a giant phehistoric dinosaur), Guiron (a knife-headed extraterrestrial demon beast) and finally Barugon (a enormous lizard whose tongue sprays a freezing liquid that can freeze things solid and a massive back which emits a powerful rainbow energy ray that can melt or dissolve any hard solids). Gamera self-destructs in the end to destroy Zanon once and for all and protect the earth.