The Japanese fishing boat Eikō-Maru is attacked by a flash of light from the water near Odo Island and sinks. A rescue boat, the Bingo-Maru, is sent out to investigate the accident, but meets the same fate. A second search boat is sent out and finds a few survivors in the area, and like the other two boats, is shipwrecked.
Meanwhile, on Odo Island, the natives of the fishing community are unable to catch anything. An elder says that Godzilla must be the cause. According to legend, Godzilla is a kaiju who lives in the sea that comes from the ocean to feed on mankind. Whenever fishing was poor, the natives used to sacrifice girls to prevent Godzilla from attacking the village.
Later, a helicopter carrying investigative reporters arrives on Odo Island. The natives all believe that the recent disasters in the ocean were caused by Godzilla, but the reporters remain skeptical. That night the natives perform an exorcism in hopes that Godzilla will not attack again. As the natives are sleeping, a storm hits the island, and much of the village is destroyed, as though it was crushed from above. The family of Shinkichi Yamada is killed during the storm, and Shinkichi insists they were killed by a giant monster.
The next day, the witnesses are brought to the National Diet Building in Tokyo. Paleontologist Dr. Kyohei Yamane requests that an investigative party be sent to Odo Island. A ship is sent out and arrives safely on the island. Yamane finds giant footprints contaminated with radioactivity, along with a trilobite. Suddenly, the village alarm is set off and the villagers run towards the hills. Godzilla pops his head over the hill and roars. The villagers discover that Godzilla is too large to fight and flee for their lives. Godzilla then leaves for the ocean.
Afterwards, Yamane starts doing some research and discovers that Godzilla is really a prehistoric hybrid of land and sea reptiles. He also discovers that the sediment from Godzilla’s footprint contained a massive amount of Strontium-90, which could have only have come from a nuclear bomb. After Yamane’s presentation, a man from the crowd suggests that the information should not be publicly known. Since Godzilla is the product of atomic weapons, the truth might cause some bad consequences, since world affairs are still fragile. However, a woman objects to Mr. Ōyama’s suggestion because the truth must be told. After she insults Ōyama, chaos breaks loose in the Diet Building.
Godzilla’s origins are then revealed to the public. An anti-Godzilla fleet is immediately sent out and uses depth charges against Godzilla, in an attempt to kill the monster. In his home, Yamane sits alone in the room with the lights out. Yamane, being a zoologist, does not want Godzilla to be killed, but rather, studied.
That night, Godzilla suddenly rises in Tokyo Bay in front of a party ship. Within a minute, the monster descends back into the ocean, but his brief appearance causes nationwide panic. The next morning, officials ask Yamane if there is a way to kill Godzilla. A frustrated Yamane explains that Godzilla has already survived a massive amount of radiation, and believes that he should be studied to see what keeps him alive.
Yamane’s daughter, Emiko Yamane, is engaged to Dr. Daisuke Serizawa, a colleague of Yamane’s. Emiko, however, is in love with Lieutenant Hideo Ogata of the Nankai Steamship Company. When Emiko visits Serizawa to tell him that she loves Ogata, and wishes to break off her engagement to him, Serizawa reveals to her his own dark secret. He had unintentionally created a device that can destroy all life in the sea while performing experiments with the element oxygen. This device is called the Oxygen Destroyer, and is more powerful than any nuclear weapon. He gives Emiko a demonstration in his lab, by using the device in a fish tank. All the fish are disintegrated, only leaving skeletons. Shocked by this discovery, Emiko leaves Serizawa, promising not to tell anybody what she witnessed. She was unable to tell Serizawa about Ogata, or that she wanted to break the engagement.
That night, Godzilla appears again out of Tokyo Bay and attacks the city of Shinagawa. While the monster’s attack is relatively short, it causes much destruction and death. The next morning, the military hastily constructs a line of 40 meter electric towers along the coast of Tokyo that will send 300,000 volts of electricity through Godzilla, should he arrive again. Civilians are then evacuated from the city and put into bomb shelters. The military then prepares a blockade along the fence line.
When night falls, Godzilla surfaces from Tokyo Bay again. The monster easily breaks through the giant electric fence, with no pain inflicted. The bombardment of shells from the Japanese army also has no effect. As Godzilla breaks through the high-tension wires, he uses his atomic breath to melt the electric fences. The tanks and military are useless against Godzilla, who continues his raid well into the night. By the end, the city is destroyed and thousands of innocent civilians are dead, dying, or wounded. As Godzilla wades into the sea, a squadron of jets fire rockets at the monster but Godzilla is unscathed as he descends once again into Tokyo Bay.
The next morning, the city is in absolute ruins. The fires started by Godzilla spread throughout the night, and completely burned the remaining parts of the city to the ground. Hospitals are overrun with victims, many exposed to heavy doses of radiation. As Emiko sees the many victims of Godzilla’s attack, she takes Ogata aside and tells him Serizawa’s dark secret, in hope that together, they can convince Serizawa do something against Godzilla.
Ogata and Emiko visit Serizawa to ask that they use the Oxygen Destroyer against Godzilla. Terrified, Serizawa refuses and storms down to his basement to destroy the Oxygen Destroyer. Ogata and Emiko follow him down in order to prevent him from doing so. However, this only results in a short fight between Ogata and Serizawa, with Ogata receiving a minor head wound. As Emiko treats the wound, Serizawa apologizes. Ogata tries to convince Serizawa that he is the only one who can save the world.
Serizawa says that even though stopping Godzilla is a priority, if the Oxygen Destroyer is used even once, even if it’s for good, politicians of the world would demand his plans, to weaponize it’s power to use for war, which could cause worldwide devastation, just like what the Atomic Bomb if a nuclear war ever started. Ogata acknowledges Serizawa’s opinion but says that if they don’t do anything, millions more innocent people will die at the hands of Godzilla.
Just then, a grim television program appears on the air, showing the devastation and deaths caused by Godzilla, along with prayers for hope and peace. Heartbroken and horrified by what he’s witnessing, Serizawa ultimately decides to use his last Oxygen Destroyer, but only one time. Serizawa then proceeds to destroy his research, knowing that this weapon was almost as dangerous and destructive as Godzilla himself, and that destroying this weapon will be for the betterment of society.
The next day, a navy ship takes Ogata and Serizawa to plant the device in Tokyo Bay. Serizawa requests that he be put in a diving suit to make sure the device is used correctly. Ogata at first refuses, but soon gives in. Ogata and Serizawa then descend into the water, and find Godzilla resting. Seemingly unaware of the divers, the monster slowly walks around the ocean floor. Ogata then is pulled back to the surface while Serizawa activates the Oxygen Destroyer. As Serizawa watches Godzilla dying from the destructive weapon, he cuts his cord and dies with Godzilla, sacrificing himself so that his knowledge of the horrible weapon dies with him. A dying Godzilla surfaces, lets out a final roar, and sinks to the bottom, disintegrating.
Although Godzilla is destroyed, the tone is still grim. As the people aboard the ship look to the sun and salute the sacrifice of Serizawa, Yamane suggests that it is unlikely Godzilla was the last of his species. He says that if nuclear testing continues, another Godzilla will probably appear somewhere in the world again.