When the Japanese freighter Eiko-maru is destroyed near Odo Island, another ship—the Bingo-maru—is sent to investigate, only to meet the same fate with few survivors. A fishing boat from Odo is also destroyed, with one survivor. Fishing catches mysteriously drop to zero, blamed by an elder on the ancient sea creature known as "Godzilla". Reporters arrive on Odo Island to further investigate. A villager tells one of the reporters that something in the sea is ruining the fishing. That evening, a storm strikes the island, destroying the reporters' helicopter, and Godzilla, briefly seen, destroys 17 homes and kills nine people and 20 of the villagers' livestock.
Odo residents travel to Tokyo to demand disaster relief. The villagers' and reporters' evidence describes damage consistent with something large crushing the village. The government sends paleontologist Kyohei Yamane to lead an investigation on the island, where giant radioactive footprints and a trilobite are discovered. The village alarm bell is rung and Yamane and the villagers rush to see the monster, retreating after seeing that it is a giant dinosaur. Yamane presents his findings in Tokyo, estimating that Godzilla is 50 m tall and is evolved from an ancient sea creature becoming a terrestrial creature. He concludes that Godzilla has been disturbed by underwater hydrogen bomb testing. Debate ensues about notifying the public about the danger of the monster. Meanwhile, 17 ships are lost at sea.
Ten frigates are dispatched to attempt to kill the monster using depth charges. The mission disappoints Yamane, who wants Godzilla to be studied. When Godzilla survives the attack, officials appeal to Yamane for ideas to kill the monster, but Yamane tells them that Godzilla is unkillable, having survived H-bomb testing, and must be studied. Yamane's daughter, Emiko, decides to break off her arranged engagement to Yamane's colleague, Daisuke Serizawa, because of her love for Hideto Ogata, a salvage ship captain. When a reporter arrives and asks to interview Serizawa, Emiko escorts the reporter to Serizawa's home. After Serizawa refuses to divulge his current work to the reporter, he gives Emiko a demonstration of his recent project on the condition that she must keep it a secret. The demonstration horrifies her and she leaves without mentioning the engagement. Shortly after she returns home, Godzilla surfaces from Tokyo Bay and attacks Shinagawa. After attacking a passing train, Godzilla returns to the ocean.
After consulting international experts, the Japanese Self-Defense Forces construct a 30 m tall and 50,000 volt electrified fence along the coast and deploy forces to stop and kill Godzilla. Dismayed that there is no plan to study Godzilla for its resistance to radiation, Yamane returns home, where Emiko and Ogata await, hoping to get his consent for them to wed. When Ogata disagrees with Yamane, arguing that the threat that Godzilla poses outweighs any potential benefits from studying the monster, Yamane tells him to leave. Godzilla resurfaces and breaks through the fence to Tokyo with its atomic breath, unleashing more destruction across the city. Further attempts to kill the monster with tanks and fighter jets fail and Godzilla returns to the ocean. The day after, hospitals and shelters are crowded with the maimed and the dead, with some survivors suffering from radiation sickness.
Distraught by the devastation, Emiko tells Ogata about Serizawa's research, a weapon called the "Oxygen Destroyer", which disintegrates oxygen atoms and causes organisms to die of a rotting asphyxiation. Emiko and Ogata go to Serizawa to convince him to use the Oxygen Destroyer but he initially refuses, explaining that if he uses the device, the superpowers of the world will surely force him to construct more Oxygen Destroyers for use as a superweapon. After watching a program displaying the nation's current tragedy, Serizawa finally accepts their pleas. As Serizawa burns his notes, Emiko breaks down crying.
A navy ship takes Ogata and Serizawa to plant the device in Tokyo Bay. After finding Godzilla, Serizawa unloads the device and cuts off his air support, taking the secret of the Oxygen Destroyer to his grave. Godzilla is destroyed, but many mourn Serizawa's death. Yamane believes that if nuclear weapons testing continues, another Godzilla may rise in the future.
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