Haru Yoshioka is a quiet and shy high school student who has a suppressed ability to talk with cats. One day, she saves a cat from being hit by a truck on a busy road. The cat she saved turns out to be Lune, Prince of the Cat Kingdom. As a thanks, the cats give Haru gifts of catnip and mice, and she is offered the Prince's hand in marriage. Her mixed reply is taken as a yes.
Wanting none of this, Haru hears a kind, female voice, which tells her to seek out Muta, a large white cat and to get directions to the Cat Bureau from him. Muta leads her there to meet Baron Humbert von Gikkingen (the same Baron from Whisper of the Heart), who is a cat figurine given life by the work of his artist, and Toto, a stone raven who comes to life much like the Baron. Soon after meeting them, Haru and Muta are forcefully taken to the Cat Kingdom, leaving Toto and the Baron in the human world to follow the group from the air; they find the entrance to the Cat Kingdom on Earth: five lakes forming a cat's paw.
Haru is treated to a feast at the castle of the Cat King. She begins to slowly turn into a cat (with tan paws, ears, nose, tail, and whiskers; for a second, she also gets fangs), though she still remains mostly human. The King hopes that she will make a suitable bride for the Prince. At the feast, the Baron (in disguise) dances with Haru as part of the entertainment. He reveals to her that the more she loses herself in the kingdom, the more cat-like she will become, and that she has to rediscover her true self. When the Baron is discovered and is forced to fight the guards, he and Haru are helped by Yuki, a white female cat who works as a servant in the palace and had previously tried to warn Haru to leave the Cat Kingdom. After Yuki shows them an escape tunnel, Haru, the Baron, and Muta move through a maze to a tower, which contains a portal to Haru's world. The King goes through a series of efforts to keep them in the kingdom long enough for Haru to remain trapped in her cat-like form; his ultimate plan is still to force her to become his daughter-in-law.
Prince Lune and his guards return to the Cat Kingdom, revealing the King was not acting on his behalf and that he has no desire to marry Haru; he has instead planned on proposing to Yuki. Muta is revealed to be Renaldo Moon, a notorious criminal in the Kingdom (having devoured a whole lake of fish in one session). Haru learns that the strange voice who had advised her to go to the Cat Bureau was Yuki's. In her childhood, Haru had saved Yuki from starvation by giving her the fish crackers she was eating, and thus, Yuki has now repaid her kindness. After she rejects the King's marriage proposal outright, Muta tells Haru, "I respect a woman who stands up for herself". He then proceeds to help her escape from the King's soldiers.
Eventually, the Baron, Haru and Muta escape the cats' realm, with the aid of Prince Lune and Toto, and Haru discovers her true self, telling the Baron how much she has come to like him. He tells her the doors of the Cat Bureau will be open for her again if the need ever arises. Haru returns to the human world with more self-confidence; after learning from her friend, Hiromi, that her former crush has broken up with his girlfriend, she simply replies "it doesn't matter anymore."