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In July 2002, Agent J has become a top agent but has developed a reputations for neuralyzing partners he feels aren't emotionally able to cope with the work. When he is called to investigate the murder of an alien, Ben, at his pizzeria, waitress Laura Vasquez tells him that the murderers are Serleena, a shapeshifting, worm-like Kylothian who has taken the form of a Victoria's Secret lingerie model, and her two-headed servant Scrad and Charlie. Laura says they were looking for something called the Light of Zartha. J is strongly attracted to Laura, and in violation of MiB rules, does not neuralyze her to erase her memories.

J finds that little is known about the Light of Zartha, except that it is immensely powerful. As he investigates the crime, every lead points to his former partner and mentor, Agent K, who was neuralyzed upon retirement five years previously and remembers nothing of his MIB service. In Truro, Massachusetts, where K is now the town's postmaster, J convinces him of his past by proving that all of his fellow postal workers are aliens. Back in New York City, Serleena, along with Scrad and Charlie, launches an attack on MIB headquarters before K's neuralyzation can be reversed, but Jack Jeebs has an illegal deneuralyzer in his basement. K eventually regains his memories, but remembers that years before, he neuralyzed himself specifically to erase what he knew of the Light of Zartha and those memories have not returned. As a precaution, he left himself a series of clues.

At the pizzeria, they find a locker key. J and K fear for Laura's safety and hide her with the worms. The key opens a locker in Grand Central Station where a society of tiny aliens, who worship K as their deity, guard their most sacred relics: K's wristwatch and video store membership card. At the store, as J and K watch a fictionalized story of the Light of Zartha, K remembers the Zarthan Queen Lauranna long ago entrusted Men in Black with safeguarding the Light from her nemesis, Serleena, who followed Lauranna to Earth and killed her. After hiding the Light, a grief-stricken K neuralyzed himself, to bury his sadness, and to ensure that he would never reveal its hiding place. K still cannot remember where he hid it nor what the Light actually looks like. Thinking it might be Laura's bracelet, he only remembers that it must return to Zartha soon or else both Earth and Zartha will be destroyed.

At the worms' apartment, they find that Laura has been captured by Serleena. With the worms, they counterattack MIB headquarters, freeing Laura and the other agents. Serleena attempts to retaliate by chasing them with a spaceship through New York but is eaten by Jeff, a gigantic worm alien living in the New York City Subway.

Laura's bracelet leads J and K to the roof of a skyscraper where a ship stands ready to transport the Light back to Zartha. K reveals that Laura is the daughter of Lauranna (and, it is implied, K's daughter) and that she's also the Light. K convinces J and Laura that she must go to Zartha to save both her planet and Earth from destruction. Serleena, who has absorbed Jeff and taken his form, attempts to snatch the ship carrying Laura as it lifts off, but J and K blast her out of the sky. Since all of New York City has just witnessed this battle in the skies over the metropolis, K activates a giant neuralyzer in the torch of the Statue of Liberty.

Back at MIB headquarters, J finds that K and Chief Zed have relocated the tiny locker-dwelling aliens to his Men in Black locker hoping to give him some perspective. When J suggests showing the miniature creatures that their universe is bigger than a locker, K shows J that the human universe is itself a locker within an immense alien train station.

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