Eleven-year-old Gregor is left home alone in his family's New York City apartment to watch his sisters and grandmother. When his baby sister Boots falls through an old air duct grate in the basement, he dives in after her. The two fall miles below into the Underland, a subterranean world inhabited by humans with near-translucent skin, violet eyes, and silver hair, as well as giant sentient bats, rodents, and insects. There, an escalating conflict is unfolding between the human kingdom of Regalia and the rats led by King Gorger. Gregor and Boots meet several Underlanders, including the crown princess Luxa, her cousin Henry, and the bats who are bonded to them as warrior allies. At first, Gregor only wants to return home, but after being attacked by rats and saved by the Underlanders, he becomes entangled in their conflict. He soon learns of a prophecy written by Bartholomew of Sandwich, which foretells that an Overland warrior will stop the rats’ attempt to take over the Underland. The Regalian council believes Gregor is this warrior and urges him to undertake a quest. Although hesitant, Gregor agrees after discovering that his missing father had also fallen into the Underland years earlier and is now a prisoner of the rats.

Gregor, Boots, and a group of Regalians set out to rescue his father and recruit allies for the coming war. Along the journey, they face dangerous creatures such as giant spiders and scorpions, while being guided at times by the rebel rat Ripred. Eventually, they find Gregor’s father, weak and tortured in King Gorger’s prison. During the rescue attempt, Henry reveals that he has been secretly helping the rats, hoping to form an alliance and eliminate weaker species. As the group tries to escape, Gregor sacrifices himself to lure the enemy forces toward a cliff. In the chaos, Ares chooses to save Gregor instead of Henry, leading to the deaths of King Gorger, Henry, and many rats. When the survivors return to Regalia, Luxa and her family are devastated by Henry's betrayal and death, and Ares is sentenced to banishment. Gregor saves him by forming a new bond. Afterward, once the Regalian doctors have treated his father as much as possible, Gregor, his sister, and his father return to the surface and reunite with their family.

|\ // /| |/ /\ | /| \ /\ /| | /\ \ /| ||/ \ /\ \\ \ || |/ \ /\ /| | /\ \ |/ |\ // /| |/ /| // |||/ // //

||/ // |/ \ /\ /| |/ /| \ /\ /| \ /\ // /| \ ||/ |/ /| ||/ /| //

|/ /| |/ \ /\ /| |/ \ ||/ /| \ /\ |/ /| ||/ |/ /| /\ /| \ /\ /| \ /\ |/ /| /\ /| |/ \ ||/ |/ /| /\ /| \

|/ /\ |/ \ /| // ||/ |/ /| |/ /\ /| |/ \ ||/ |/ /| |/ \ /\ /| |/ /\ |/ \ /| // ||/ |/ /| /\ /| \ /\ /| |/ \ ||/ |/ /| /\ /| \ /\ /| |/ \ ||/ |/ /| /\ /| \