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The film begins with a large tidal wave, triggered by a distant explosion, which threatens to drown the island of Atlantis. In the midst of an evacuation from the capital city, the Queen of Atlantis is caught by a strange, hypnotic blue light and lifted up into the "Heart of Atlantis", a powerful crystal protecting the city. The crystal consumes her and creates a dome barrier that protects the city's innermost district. She leaves behind a young daughter, Princess Kida, and husband, King Kashekim Nedakh, as the island sinks beneath the ocean.
Nearly nine thousand years later in 1914, Milo Thatch —a cartographer and linguist at the Smithsonian Institution who is marginalized for his research on Atlantis—believes that he has found the location of The Shepherd's Journal, an ancient manuscript allegedly containing directions to the lost island. Hubie, Marina, Rocko, Petra, Beanie, Timmy, Pikatwo, Bonkers, Fawn and Buck are the only ones who believe his theories.
After his proposal to search for the Journal is rejected by the museum board, a mysterious woman, Helga Sinclair, introduces Milo, Hubie and the others to Preston B. Whitmore, an eccentric millionaire. Whitmore has already funded a successful effort to retrieve the Journal as repayment of a debt to Milo's grandfather, and recruits Milo, Hubie and his friends to lead an expedition to Atlantis as soon as he deciphers it.
The expedition departs with a team of specialists led by Commander Rourke, who also led the Journal recovery expedition. The crew includes Vinny, a demolitions expert; Mole, a geologist; Dr. Sweet, a medical officer; Mrs. Packard, a radio operator; Audrey, a mechanic; and Cookie, a mess cook. They set out in the Ulysses, a massive submarine, but are soon attacked by the monstrous Leviathan, a robotic lobster-like creature that guards Atlantis' entrance. The Ulysses is destroyed, but Milo, Rourke, Hubie, Marina, their friends and part of the crew escape and make their way to an underground cavern described in the Journal as the entrance to Atlantis.
After traveling through a network of caves and a dormant volcano, the team reaches Atlantis. They are greeted by Kida — who, despite her age, resembles a woman in her early 20s — and discover that the Atlantean language is the basis of many existing languages which allows the Atlanteans to understand English. Kida enlists Milo's aid in deciphering the Atlantean written language, long forgotten by the natives. By swimming deep within the city's submerged ruins and translating underwater murals, Milo, Hubie and Marina help Kida uncover the nature of the Heart of Atlantis: it supplies the Atlanteans with power and longevity through the crystals worn around their necks. Milo is surprised this is not mentioned in the Journal, but upon examination realizes a page is missing.
Returning to the surface with Kida, Milo, Hubie and Marina discover Rourke has the missing page. Rourke and the crew betray Milo' kidnap Hubie's friends and plan to bring the Crystal to the surface and sell it. Rourke mortally wounds the King of Atlantis while trying to extract information about the crystal's location, but finds its location for himself hidden beneath the King's throne room. The crystal detects a threat and merges with Kida. Rourke and the mercenaries lock Kida in a crate and prepare to leave the city. Knowing that when the crystal is gone the Atlanteans will die, Milo and Hubie berate the crew for betraying their consciences and ultimately convinces them to leave Rourke and remain in Atlantis. The King explains to Milo that the crystal has developed a consciousness; it will find a royal host when Atlantis is in danger. He admits that he tried to use it as a weapon, but the crystal's powers were too great to control, thus leading to the tidal wave that destroyed the city. This lead to his decision to hide it as a precaution to ensure history would not repeat itself, and prevent Kida from meeting the same fate as her mother. He warns Milo that if Kida remains bonded to the Heart of Atlantis, she will be lost to it forever. As he dies, he gives his crystal to Milo, telling him to save Kida and Atlantis. Encouraged by Sweet, Milo rallies Hubie, Marina, Rocko, Petra, Beanie, Timmy, Pikatwo, Bonkers, Fawn, Buck, the crew and the Atlanteans to stop Rourke.
In a battle inside the volcano, Helga and the other mercenaries are defeated including Rourke, who is killed when Marina slashes his arm with a crystal shard (which gradually turns him to crystal), and then collides with his air ship's propellers. As Milo, Hubie and the others fly the crystal back to the city, the volcano erupts. With lava flowing towards the city, Kida (in her crystal form) rises into the air and creates a protective shield. The lava breaks away harmlessly, showing a restored Atlantis, and the crystal returns Kida to Milo.
The surviving crew members are rewarded with gold, (Hubie and his friends refuse) return to the surface and promise to keep the discovery of Atlantis a secret. Milo, having fallen in love with Kida, stays behind to help her rebuild the lost empire.
- This film will be dedicated to James Garner (April 7, 1928 – July 19, 2014) who died of a heart attack.