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Synopsis
Sailor Pietro and his rat companion Roscuro dock in the kingdom of Dor, famous around the world for its delicious soups, during the "Royal Soup Day." The chief cook, Chef Andre, makes good soup due to Boldo, a magical genie that emerges from his pot and is made entirely out of food. Enchanted by the smell of the delicious soup, Roscuro slips away and ends up in the royal banquet hall, on a chandelier above the royal family's table. He slips and falls into the Queen's soup, giving her such a fright that she has a heart attack and dies.
The entire hall goes into panic, as the guards pursue Roscuro. He attempts to flee the castle but sees Pietro's ship has already sailed away. He narrowly escapes capture by falling down a sewer drain, which leads to the castle dungeons, where he's found and taken in by Botticelli, the leader of the dungeon's large rat population.
Distraught over his wife's death, the king forbids any and all things related to soup and makes rats illegal. Without its soup, Dor becomes impoverished and dreary. Andre is banned from making any more soup and Boldo stops appearing. The king's daughter, Princess Pea, despairs over the sad state of the kingdom and how her father has shut out both her and the world in his grief.
In a mouse village in the castle's abandoned kitchen storage room, a baby is born to the Tilling family. They name him Despereaux. As he grows up, it becomes clear Despereaux's not like other mice: he isn't meek and timid, but brave and curious, unnerving his family, friends, and school teachers. In an effort to teach him to behave like a proper mouse, his brother Furlough takes him to the castle library to show him how to chew books, but Despereaux is more interested in reading than eating them.
He becomes fascinated by fairytale books about daring knights and trapped princesses. One day while reading, he comes across Princess Pea and the two speak. She makes him promise to finish reading the story about a trapped princess so he may tell her how it ends. Upon discovering Despereaux has violated mouse law by talking to a human, his parents turn him in to the mouse council.
The council banishes Despereaux to the dungeons, where he meets and tells the princess' story to the castle jailor, Gregory, but he doesn't listen and leaves Despereaux alone. There, he is captured by the rats and thrown into their arena with a cat. As Despereaux is about to be eaten, Roscuro saves his life by asking Botticelli to give Despereaux to him to eat. Having been unable to adjust to being a sewer rat, Roscuro is desperate to hear about the outside world. The two become friends, as every day Despereaux tells him the stories and of the princess and her sadness.
Hoping to make amends for all the trouble he's caused, Roscuro sneaks up to Princess Pea's room and tries to apologize, but she's frightened by him and lashes out. Hurt by this, Roscuro decides he wants to hurt Pea. He enlists the help of Miggery "Mig" Sow, Princess Pea's slightly deaf young maid who longs to be a princess herself, by convincing her she can take Pea's place if she kidnaps her. After Mig drags Pea down to the dungeons, Roscuro double-crosses her and locks her in a cell.
Meanwhile, Despereaux (who has been punished by the mouse council again for his bravery by learning to be afraid by the threadmaster, Hovis, but after being lost in a cave, the mice thought he was dead) realizes that the princess is in danger, he tries to tell the king but he was too despondent to listen. Despereaux tries to get help elsewhere; he tries to tell his people to help, but they are afraid to see him alive (thinking that he is a ghost.) So Despereaux decides to ring the town's bell to prove to his people that he is still alive. A sleeping Andre heard the bell and dreams of his days before soups were illegal. After dreaming, Andre decided that he had enough of this law and gets back to make some soup, which brings the enchanted smell back to the kingdom and brings back Boldo.
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. Back at the castle, Despereaux tried to get help from Andre and Boldo, but Andre doesn't listen. Boldo, wanting to help, turns into a knight by Despereaux. As for Roscoro, he figures out that Botticelli is a double-crossing traitor and that Pea is doomed. However, Boldo sacrifices himself against the rats to let Despereaux escaped them and lets loose a cat and brings sunshines to the rat world, and the rats run away. As the cat runs back to its cage, Roscuro then forces Botticelli into it, where he is eaten by the cat.
Mig is later reunited with her long-lost father Gregory, who recognizes the heart-shaped birthmark on the back of her neck. It finally stops raining and the sun shines after soup is made for the first time in years. The mice all then try to be braver like Despereaux. The king is able to overcome his grief and soup and rats are allowed back in the kingdom. Roscuro returns to a life at sea, where there is always light and a gentle breeze and Despereaux himself takes off on a journey to see the world as the film ends.