Larry Daley (Ben Stiller) is a divorced father who is unable to keep a stable job, the bulk of his career consisting of failed business ventures. He is desperate to win the support of his son Nick (Jake Cherry), whom he fears is beginning to look up to his more successful future stepfather, Don (Paul Rudd), a bond trader on Wall Street. Larry goes to a job agency and is sent to the American Museum of Natural History, where he is hired as a night guard. The three elder (soon to be retired) night guards, Cecil (Dick Van Dyke), Gus (Mickey Rooney), and Reginald (Bill Cobbs), give him a quick tour, advise him to leave some of the lights on, and warn him not to let anything “in…or out”, which Larry meets with humorous skepticism. Once night comes, Larry discovers that the museum exhibits come to life, including a living Tyrannosaurus rex skeleton, a mischievous capuchin monkey named Dexter, miniatures led by cowboy Jedediah (Owen Wilson) and Roman General Octavius (Steve Coogan), an Easter Island head obsessed with “gum-gum” and a wax model of Theodore Roosevelt (Robin Williams).
Roosevelt explains to Larry that an Egyptian artifact — the Tablet of Akmenrah — was brought to the museum in 1952, and on that night, everything in the museum came to life, and each night since. However, if the exhibits are outside of the museum during sunrise, they turn to dust. Roosevelt helps Larry by restoring order (insisting it is the only time he will help), and while unnerved, Larry decides to remain as a guard. On Cecil’s advice, Larry begins to study the history of the events and people in the exhibits to prepare himself better for their animation. He introduces himself to the museum tour guide, Rebecca Hutman (Carla Gugino), who is writing a dissertation on the life and times of Sacagawea (Mizuo Peck). Larry learns much of the history of the various exhibits from Rebecca. The next night, Larry uses what he has learned to better control the exhibits, but again fails when four Neanderthals set fire to a display, and one is turned to dust when he leaves the museum at the dawn. Larry barely manages to keep his job after the museum’s director, Dr. McPhee (Ricky Gervais), discovers the mess. Larry tries to tell Rebecca about what happens to the exhibits at night, even offering to let her meet Sacagawea to help with Rebecca’s dissertation, but she does not believe him and leaves in tears, convinced that Larry was making fun of her.
Larry brings Nick to the Museum, but fails to impress him when nothing comes to life. They find Cecil, Gus, and Reginald stealing the Tablet of Ahkmenrah. Cecil then reveals that, like the museum exhibits, the guards receive enhanced vitality and energy from the Tablet. Unwilling to forsake it, the three intend to steal the tablet, along with various other museum artifacts to fund their retirement, and frame Larry for the theft. Nick activates the tablet’s power and brings the exhibits to life once more, but then Cecil locks the two in the Egyptian room and flees with the tablet. Larry releases the mummy of Pharaoh Ahkmenrah (Rami Malek) from his sarcophagus: surprisingly Akmenrah speaks English, having spent many years as an exhibit in the Egyptology Department at Cambridge University. Akmenrah then tells his jackal-headed “guards” to let them out. The three find the other exhibits fighting, and Larry, after the Easter Island head manages to get their attention, convinces them to work together to reclaim the tablet or else lose their ability to be animated.
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