Megamind (Will Ferrell) is a super-intelligent alien who — at only eight days old — is sent to Earth by his parents as his home planet is destroyed by a black hole. However, he lands in the Prison for the Criminally Gifted at Metro City, thanks to another infant alien similarly sent from a different planet who eventually becomes a superhero known as Metro Man (Brad Pitt), defender of the fictional Metro City. As a result, Megamind is raised as a social deviant, who is neglected for his destructive intellect, with his piranha-like sidekick Minion (David Cross) as his only friend. Realizing that he is only gifted in causing trouble, and jealous of all of the attention and praise young Metro Man receives, Megamind becomes a supervillain to rival Metro Man, though he is thwarted on a regular basis, despite being assisted by Minion and an army of "Brainbots".
During one of his many attempts to defeat Metro Man, Megamind kidnaps news reporter Roxanne Ritchi (Tina Fey) and uses her as bait to lure Metro Man into the city observatory where Megamind intends to kill him with a death ray. The plan appears flawed enough for Metro Man to escape, but he proclaims that the inside of the observatory is lined with copper, which he says drains his power. Metro Man is then seemingly killed by the death-ray. Megamind is initially thrilled that he has defeated his archenemy, and he proceeds to live the criminal dream life, taking over town hall and plundering the city. His happiness more of an assumption than a reality, he soon grows depressed over the fact that without someone to fight, his life as a supervillain no longer has any purpose.
Megamind runs into a museum curator named Bernard (Ben Stiller) while destroying the Metro Man Museum and trying to avoid Roxanne, and disguises himself as him, dehydrating the real Bernard. Roxanne and Megamind disguised as Bernard leave the building before it is destroyed. Megamind disguised as Bernard begins dating Roxanne, and she inspires him to create a new superhero to fight using a serum of Metro Man's DNA. Hoping to uncover any evil plans Megamind has for the city, Roxanne breaks into Megamind's lair and fights with him over a syringe gun containing the serum, which is accidentally fired and injected into Roxanne's cameraman Hal Stewart (Jonah Hill). Megamind manipulates Hal into becoming a superhero named Tighten under the guide of being "space dad", but at the same time falls in love with Roxanne and begins dating her while disguised as Bernard. Tighten attempts to use his powers to woo Roxanne, but is quickly spurned and grows jealous of the Bernard-disguised Megamind. Megamind soon begins having second thoughts about being a villain, finding more enjoyment pursuing a relationship with Roxanne. Minion discovers the relationship, quarrels with Megamind over it, claiming that "the bad guy doesn't get the girl!" Frustrated, Megamind then yells that he doesn't want to be the "bad guy" anymore and tells Minion to go, telling Minion that he doesn't need him. Saddened, Minion leaves, their friendship apparently lost.
After Roxanne kisses "Bernard" on a date, Megamind's identity is accidentally exposed when Roxanne unintentionally deactivates his holowatch, causing Roxanne to reject him as she is unable to reconcile his past evil deeds with his real, more empathetic temperament. Heartbroken, Megamind follows through with his plan to fight Tighten. By this time, Tighten has decided he would rather be a supervillain. Hal is socially awkward, and it is assumed he has lived a life of mediocrity. Resentful of life and perceived apathy, Hal as Tighten expresses his psychology by stealing money, art, video games, surfboards and a big screen TV and saying it is too much work to be a hero. Disgusted, Megamind provokes Tighten by revealing he is both the "space dad" and Bernard. Utterly furious that the "intellectual dweeb" stole Roxanne, Hal attacks with a vengeance-but unlike Metro Man, Tighten has no qualms with outright killing Megamind, and Megamind is forced to flee for his life. With nobody to stop him, Tighten begins wreaking havoc in Metro City in revenge for Roxanne spurning him and all who'd ever called him a loser.
Megamind attacks Tighten with a copper sphere, but is shocked to see Tighten escape the copper sphere with one punch. Confused about this inconsistency, Megamind convinces Roxanne to search for clues about his weaknesses in Metro Man's old hideout. There, they discover that Metro Man is still alive and learn that he faked his death (and his weakness to copper) so that he could retire from being a superhero—having realized that he'd lived his entire life without ever actually making a choice about what he really wanted—and live his true passion: music. Megamind and Roxanne try to persuade Metro Man to defeat Tighten, but he refuses. Roxanne and Metro Man instead prompt Megamind to fight, but he refuses, claiming that he's not a hero and "I don't get the girl." He instead turns himself in to his regularly attended prison. When Tighten kidnaps Roxanne, however, Megamind is broken out of prison by Minion (disguised with the holowatch as the warden of the prison, and only lets him out and reveals himself after he gets an apology) and goes to save her. Minion, disguised as Megamind, rescues Roxanne but is wounded in the process. Metro Man then miraculously shows up, but is actually Megamind in disguise. He manages to intimidate Tighten into fleeing the city, until he accidentally calls Metro City "Metrocity", as he always has. After taking a beating from Tighten, Megamind defeats him by using the Defuseer Gun to drain Metro Man's DNA from his body, and thus stripping him of his powers. Hal ends up in Megamind's former prison cell, while Megamind is embraced by Metro City as its new defender. Roxanne accepts Megamind and he "gets the girl," having proved himself a true hero. Megamind decides he is deeply satisfied with his new role as the hero and Roxanne's beau, as a disguised Metro Man silently congratulates him.
A post-credits scene shows Minion doing the laundry, only for Bernard—who was "de-hydrated" by one of Megamind's weapons and turned into a small cube—to pop out of the washing machine claiming that this was the worst day of his life; Minion then responds and whacks him with a forget-me-stick.
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