A ship sails into the kingdom of Dor, known for its 'Royal Soup Day.' Roscuro (Dustin Hoffman), a rat, is aboard with a human companion, Pietro.
Roscuro is mesmerized by the aroma of soup being prepared in the castle's kitchens and he escapes Pietro to find the source. In doing so, he finds the castle banquet room and accidentally falls into the Queen's soup after she takes the first sip. The Queen then has a heart attack, falls headfirst in her soup bowl and eventually drowns with no one noticing. Meanwhile, Roscuro is being chased about the castle. The chase finally ends when Roscuro falls into a vent and plunges into the dungeons.
The king in his grief orders soup to be forbidden and rats banished, These were the Dark Ages and the town falls into eternal darkness and famine. Roscuro, meanwhile, meets Botticelli (Ciarán Hinds), the brutal leader of the rat world.
A few years later, an adventurous mouse, Despereaux Tilling (Matthew Broderick) is born, and becomes friends with the lonely Princess Pea (Emma Watson). Upon finding out that Despereaux has broken the law by speaking with a human, the Mouse Council banishes him to the dungeons, from where he is saved by Roscuro from being eaten by the other rats. Despereaux tells Roscuro of the princess's gloom, which touches the rat.
Roscuro approaches the princess to apologize, but she is terrified of him and he is chased out. Hurt, he decides to kidnap the princess. He enlists the help of a servant girl, Miggery Sow (Tracey Ullman), whom he later double crosses, and locks in a cell.
Meanwhile, Despereaux realizes that the princess is in danger. Back in the rat colony, Roscuro sees the apologetic sincerity in Pea's eyes and regrets his actions, but is unable to stop the rats, to whom he has given her, from clambering over her. Roscuro tries to tell the rats that Pea is not bad, but Botticelli does not let him because he wants Pea dead, even going as far as allowing the rats to eat or trample over Pea. Roscoro figures out that Botticelli is a double-crossing traitor and that Pea is doomed. However, little Desperaux lets loose a cat, and the rats run away before the cat goes back into its cage. Roscuro then makes Botticelli go into the cage, where he is eaten by the cat.
Miggery is rescued by the jailer, who is revealed to be her father, and goes back to her farm with him. Roscuro is reunited with Pietro, and the princess and the king decide to soothe their grief by relying on each other for support. The mice no longer live in fear, and Despereaux, reunited with his family, remains close friends with the princess even as he departs for his next adventure.
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