In the Victorian-era town of Cheesebridge, a community thrives on rumors of nefarious creatures known as Boxtrolls, who allegedly come out at night to steal cheese and children. The town's cheese-obsessed elite employ a villainous exterminator named Archibald Snatcher to eradicate the supposed menace. Unbeknownst to the townsfolk, Boxtrolls are in fact gentle, oddball tinkerers who wear recycled cardboard boxes as shells. They've even raised an orphaned human boy named Eggs among their ranks, underneath the cobblestone streets they call home.

Eggs, now a preteen, has grown up thinking he's a Boxtroll but begins to unravel the truth about his past when he encounters Winnie, the feisty daughter of Cheesebridge's aristocracy. Her morbid curiosity about the Boxtrolls leads her to discover Eggs' true identity. As their friendship blossoms, they decide to fight back against the Boxtroll-catcher's campaign of fear and propaganda, prompting Eggs to venture above ground. There, he must confront the damaging myths woven about his adoptive family and seek to prove that the Boxtrolls are not monsters, but misunderstood innocents who've been unjustly maligned.