Plot
During Dor's annual "Royal Soup Day", sailor Pietro and his rat companion Roscuro arrive in an enchanting medieval French kingdom renowned for its exquisite soups. Chef Andre, the kingdom's culinary maestro, crafts his delectable creations with the help of Boldo, a magical culinary genie residing in his pot. However, Roscuro's curiosity leads him to the royal banquet hall, where his accidental plunge into Queen Rosemary's soup triggers a heart attack, claiming her life. Disheartened by the tragic turn of events, Roscuro discovers that Pietro has left him behind to fend for himself in the castle's dungeons. Roscuro finds shelter with Botticelli Remorso, the enigmatic leader of Dor's rat population. However, he struggles to adapt to their warlike culture. Meanwhile, grief-stricken King Philip bans all things soup-related, declaring rats illegal. This prohibition not only prevents Andre from making his beloved soup but also drives Boldo away. Dor, devoid of the life-giving soup, slowly fades into poverty and despair. Princess Pea, deeply affected by her father's grief, mourns the kingdom's decline and her own isolation from the world.
In a mouse village within an abandoned kitchen storage room, Despereaux is born into the Tilling family. The newborn Despereaux is immediately noted by his family for his large ears and having been born neither blind nor crying. As he grows up, it is clear he is different from other mice; he is brave and curious rather than timid, unnerving other mice around him. In an effort to teach him to be a "proper mouse", his brother Furlough takes him to the royal library to show him how to chew books, but Despereaux is more interested in reading them, becoming fascinated by their stories. One day, Despereaux encounters Pea, promising to finish the story about a trapped princess and tell her how it ends. Upon discovering that Despereaux has violated mouse law by talking to a human, his parents, Lester and Antoinette, turn him over to the mouse council to avoid blame.
The council banishes Despereaux for the crime of having courage. The "threadmaster", a blind mouse named Hovis, lowers Despereaux into the dungeons using a red thread, where he is presumed dead by the rest of the mice. In the dungeons, Despereaux tells the princess story to the jailor, Gregory, who stops listening and leaves him alone. Despereaux is captured by the rats and thrown into their arena with a tabby cat. As Despereaux is about to be eaten, Roscuro saves his life by asking Botticelli to give Despereaux to him under the pretense of eating, appearing to relent to the sewer rat dogma.
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 stories of the princess and her sadness. Wishing to make amends for the trouble he has caused, Roscuro sneaks into Pea's room and tries to apologize to her, but she lashes out at him, and guards come after him. Hurt by this, Roscuro vows revenge. He enlists the help of Miggery "Mig" Sow, Pea's young, hearing impaired maid who longs to be a princess by convincing her she can take Pea's place if she kidnaps her. After Mig drags Pea to the dungeons, Roscuro double-crosses her and locks her in a cell.
Meanwhile, Despereaux discovers that the princess is in danger, and he tries to tell the King, who is too depressed to listen. Despereaux tries to get help elsewhere; he returns to the mouse village and tries to enlist his family, but they are afraid of his presence — for he has fallen in flour, so they mistake him for returning as a ghost — so he rings the town's bell to prove his survival, but still no one comes to his aid. Andre hears the bell, reminding him of the time he made soup, and, having had enough of the law, gets back to making soup, which brings back Boldo. Despereaux tries to get help from Andre and Boldo, with limited success. As Andre is distracted by a rainy thunderstorm (which was caused by the smell of the soup being released into the sky), Boldo agrees and takes Despereaux back to the dungeons. En route, they are attacked by rats; Boldo sacrifices himself to allow Despereaux to reach the arena.
In the arena, Roscuro sees the apologetic sincerity in Pea's eyes and regrets his actions. Still, an enraged Botticelli signals the rats to eat Pea. Despereaux releases the cat to chase some of the rats away, and fights off the others. Botticelli captures Despereaux, but the rain clouds part and sunlight reflects off a lost heart-shaped locket into the dungeon, stunning the photophobic sewer rats. Roscuro saves Despereaux by using one of the arena's spotlights to direct the sunlight at Botticelli, sending him falling into the arena, where the cat chases him into its cage; Pea shuts in the both of them with her feet, leaving Botticelli to be eaten as the rest of the sewer rats flee into the shadows.
In the aftermath, Mig is reunited with Gregory, who turns out to be her long-lost father, and they return together to their farm. Meanwhile, the King overcomes his grief and allows soup and rats back into the kingdom; it stops raining, and the sun rises over Dor; Roscuro returns to his life at sea; Despereaux, who also inspired the mice to be brave just like him, departs on a journey to see the world.
