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.
Gamera destroys the American jet with his fireball and escapes into the sea. The monster heads to Japan and surfaces from Sagami Bay, where Toshio, a boy releasing his own pet turtle, sees him. Gamera destroys the city of Fujisawa and destroys a lighthouse. However, he also rescues Toshio from falling from that same lighthouse, and then retreats back into the sea. Scientists and government officials hold a conference to discuss killing the monster.
Gamera destroys a research ship, kills the crew, and then heads to Tokyo. He is attacked with freeze bombs, and blown up, falling onto his back as a result. The scientists indicate that a turtle cannot right itself once on its back, and that Gamera with therefore die of starvation. Gamera then pulls his head and limbs into his shell and flies away.
Toshio and his family decide to stay with an uncle in Tokyo because they have nowhere else to go. Toshio explains to the professor that Gamera is lonely, and like regular turtles, he is not evil. Dr. Hidaka, meanwhile, has observed that Gamera consumes fossil fuels, and may seek out atomic bombs for the energy they provide. He also emits radio signals. This leads the Japan Atomic Energy Commission to figure out what to do with its stockpiles. Meanwhile, disasters and accidents start to occur: Koto Ward is struck by flash floods, ships collide in Tokyo Bay. Dr. Hidaka claims that Gamera has caused these accidents because he is hiding in the bay.
An international scientific conference is called, and they decide to use the “Z Plan” based at Oshima Island, involving a consortium of American, Soviet, and Japanese scientists, to eradicate Gamera. Before any action can be taken, however, Gamera lands at Haneda Airport, destroying the control tower, and proceeds to wreak havoc in Tokyo (including destroying Tokyo Tower). Toshio and his family evacuate again, but Toshio disappears.
The Z Plan is still not ready, and the scientists plan to keep Gamera at bay in the meantime by confining him to an oil refinery. Dr. Hidaka has surmised that Gamera is gaining energy by consuming fires at the refinery, and they will therefore keep shipping petroleum there by train car to keep Gamera occupied for 24 hours. Toshio has found his way to the refinery and sneaks on board the train to Gamera, chased by the refinery headman, and they are both thrown from the train when it explodes. They are unharmed, and Toshio is sent on his way.
In the meantime, Plan Z is completed, and Toshio sneaks on board the ship delivering supplies to Oshima. Gamera is lured to Oshima by lighting an oil slick path From Tokyo to the island, but an oncoming typhoon blows the fire out. Aoyagi starts a bonfire, and Gamera makes his way to a volcano erupting on the island. The next day, Z Plan is put into action: Gamera is lured to a rocket and blasted off to Mars. The worldwide announcement of success extols the triumph of science over ideology, Aoyagi and Kyoko go off together, and Toshio decides he is not sad, because he is going to be a scientist so he can go visit Gamera one day.