Reporter Naoko Shindo attends a communications session with the UFO society for her television program. However, it is deemed a failure due to Naoko's skepticism. A meteor shower soon descends on Japan, with the largest meteor crashing on Mount Kurodake. Naoko's brother, Detective Shindo, is assigned to guard Princess Salno of Selgina from a political assassination during an unannounced visit to Japan. En route to Japan, an alien entity leads Salno to jump from her plane before it explodes. Professor Miura leads a research team to Mt. Kurodake to investigate the large meteor, where they discover it randomly emitting magnetic waves. Naoko is sent to investigate a prophetess claiming to be from Venus, who predicts that the pteranodon Rodan will emerge from Mount Aso.

The Prophetess catches the attention of both Shindo and Salno's uncle, both of whom recognize her as the supposedly dead Salno. Responsible for the assassination plot, Salno's uncle sends the assassin, Malmess, to kill her. After participating in a TV program, the Shobijin, Mothra's twin fairies, prepare to depart for home but are warned by the Prophetess to not sail. Naoko takes the Prophetess to a hotel to interview her, and discovers that the Shobijin have been following them, heeding the Prophetess' warning before the prehistoric sea monster Godzilla sunk their ship. After confirming that the Prophetess is Salno, Shindo finds her at the hotel and saves her from Malmess. They evacuate after Godzilla and Rodan converge on the city and battle throughout the countryside.

After psychiatrist Dr. Tsukamoto concludes that the Prophetess is human, she predicts the arrival of the alien-dragon King Ghidorah, a monster that destroyed her home on Venus. Miura and his team witness the meteor explode, unleashing the golden three-headed space dragon Ghidorah, who proceeds to attack Matsumoto. The authorities plea with the Shobijin to summon the larva monster Mothra for help, but they warn that Mothra alone could not defeat Ghidorah, and their only hope would be for Godzilla, Rodan, and Mothra to join forces. Under hypnosis, the Prophetess reveals that some Venusians escaped to Earth from Ghidorah and assimilated with humans, but at the cost of losing most of their abilities except prediction.

After Malmess overhears Tsukamoto recommending shock therapy next, he increases the voltage to a fatal degree, but fails after the power lines are destroyed by Godzilla. After thwarting Malmess and his crew, Shindo evacuates to the mountains with the Prophetess, Tsukamoto, Naoko, Miura, and the Shobijin. Mothra attempts to convince Godzilla and Rodan to set aside their differences to save the planet, but both refuse due to years of harassment from humans. However, after seeing Mothra attempt to battle Ghidorah on her own, Godzilla and Rodan change their minds and rush to her aid. The Prophetess wanders off and regains her memories after Malmess nearly kills her. Shindo manages to protectsher just in time and Malmess falls to his death. The monsters overwhelm Ghidorah and force it to flee into outer space. Prior to departing for home, Princess Salno reveals to Shindo that she has no memory as the Prophetess, but remembers the three events when Shindo saved her, and thanks him and Naoko for their help. Godzilla and Rodan watch as Mothra journeys back home with the Shobijin, who bid farewell to all.