The Tale of Despereaux is told in four separate stories called "books". Book the First tells of Despereaux's beginning, Book the Second tells of Chiaroscuro, and Book the Third is about Miggory Sow. All the characters are brought together in Book the Fourth.

A Mouse Is Born
In a castle, a tiny mouse, named Despereaux Tilling, is born to his parents Lester and Antoinette Tilling. He is the only mouse to survive his birth in his mother's litter and is born with huge ears and with his eyes open. One day, Despereaux and his brother, Furlough, find a book to eat, but Despereaux instead begins to read the words of the story about a knight saving a princess. Afterwards, Despereaux hears music and follows it to the bedroom of the Princess Pea where her father, the King, is playing guitar for her. Despereaux falls in love with the Pea causing him to go forth and speak to her.

This event is witnessed by Furlough who then tells his parents and the mouse council. Despereaux is brought on trial before the mouse council and sentenced to the dungeon, which is filled with rats. A red colored thread is placed around Despereaux's neck by the mouse threadmaster, named Hovis. However, Hovis encourages Despereaux to be brave for the Princess. Despereaux is then brought to the dungeon where he finds a long rope tied to the ankle of the castle jailer, named Gregory. Gregory protects Despereaux from the rats in return that Despereaux tell him a story.

Set before the birth of Despereaux, a rat named Chiaroscuro ("Roscuro" for short), is eating the rope at Gregory's ankle. Gregory catches Roscuro and burns his whiskers with a match. However, Roscuro is entranced by the light from the match, but another rat, named Botticelli Romorso, puts Roscuro into a trance by swinging a locket in front of his eyes. Botticelli tells Roscuro that his only purpose as a rat is to torture prisoners by pretending to be their friends only to take away the most important thing from them. Roscuro then meets a prisoner guilty for cow theft. The only thing the prisoner has with him is a red tablecloth that he got when he traded his own daughter for it along with a hen and some cigarettes. Roscuro then takes the tablecloth from the prisoner leaving him to suffer without it.

One day, Roscuro begins to explore the castle's upstairs. While there, he climbs a chandeleir during dinner and is seen by Princess Pea. She calls out to everyone to take notice that it startles Roscuro and causes him to accidentally fall into the Queen's soup tureen, causing her to have a heart attack and die. Roscuro escapes back to the dungeon along with the Queen's soup spoon. He then vows revenge on the Pea for causing the event to happen and forcing him back underground. The grief-stricken king outlaws soup throughout the Kingdom of Dor and orders for all rats to be hunted down and killed.

Gor! The Tale of Miggery Sow
Set many years before Despereaux and Chiaroscuro, a six-year-old girl named Miggery "Mig" Sow witnesses the death of her ill mother. Afterwards, Mig is sold to work by her father for some cigarettes, a hen, and a red tablecloth to a man Mig calls "Uncle". Uncle occasionally beats Mig over her ears until she goes slightly deaf and their appearance looks like cauliflower. On Mig's seventh birthday, she sees the Princess Pea riding by on horseback with her company. The Pea waves at Mig, but Mig is too surprised to wave back. When Mig does wave back, the Pea and company are already too far away. It is then that Mig decides that she too wants to be a Princess. Five years pass until the day that the king bans soup and the king's guards arrive at Uncle's house to take away with bowls and spoons. They also take Mig away from Uncle because slavery is illegal too.

Mig is then set to work in the castle where she gains much weight and begins to become lazy during her chores. One day, Mig is sent up to the Pea's room to deliver a red colored spool of thread. She gets distracted in conversation with the Pea that she is then assigned to work in the kitchen under a plump female chef named Cook. Mig is sent to the dungeons to deliver Gregory his meal and, while there, she meets Roscuro and tells him that her greatest wish is to become a princess. Roscuro plans to make Mig suffer into hearing what she wants and manipulates Mig into granting her wish if she helps him kidnap the Pea to make her become a servant girl so Mig can become a princess.

Recalled to the Light
Despereaux escapes the dungeons on the empty tray of Gregory's that Mig brings back to the kitchen, and overheard her conversation with Roscuro. However, Despereaux is soon discovered by Mig and Cook and, as he is attempting to flee, Mig chops off Despereaux's tail with a knife. Despereux then spends the night in pain, sleeping on a sack of flour. Meanwhile, Roscuro leads Mig to the Pea's room with a knife, and the two kidnapp the Pea and lead her to the dungeon.

The next morning, the castle is in a panic over the missing Princess. Guards are sent to search the dungeon, only to find Gregory dead from being lost in the dark. Despereaux is then seen by the mouse council who mistake him for a ghost because he is covered in flour. Despereaux forgives Lester for sentencing him to the dungeon and goes on to seek the King. Despereaux tells the King that he knows that Pea is in the dungeon, but the King refuses to believe him because Despereaux is a rodent, similar to a rat.

Despereaux then goes to Hovis, who gives him the entire spool of red thread and a sewing neadle for his quest to the dungeons. Despereaux cuts back through the kitchen only to see Cook making soup. However, Cook is delighted to see Despereaux because he is a mouse and not a castle guard. She gives Despereaux some soup to eat and he then makes his way to the dungeons. While there, Despereaux meets Botticelli, who tells him that he will lead Despereaux to the Pea, however, this is only an act, to make Despereux suffer.

Mig then learns that Roscuro tricked her into helping him kidnap the Pea, and that Mig will never be a princess. Roscuro plans for the Pea to remain locked in the dungeons, so that he can marvel over her brightly colored dress, but Despereaux arrives and Mig chops Roscuro's tail off with the knife. However, many rats arrive on the scene because they followed the smell of Despereaux, and the soup he recently ate. Despereaux threatens to kill Roscuro with the sewing neadle, who then begins crying. The Pea offers to Roscuro that if he lets her go, she will treat him with some soup, to which Roscuro agress. Botticelli and the other rats are disgusted by the happiness of all that is happening that they all return into the darkness.
Despereaux and the Pea become close friends. Roscuro is allowed access into the upstairs of the castle, and reunites the freed dungeon prisoner with his daughter, Mig, who is seen as a princess by him. Roscuro, Mig, the King, the Pea, and Despereaux all join together for soup, as the mice watch in amazement.

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