Plot
High-school girl Suzume Iwato lives with her aunt Tamaki in a town in Kyushu. She dreams of her childhood self walking through a ruined cityscape at night, before running into a shadowy figure resembling her late mother. One morning, Suzume meets a young man searching for abandoned locations with doors, and tells him of a nearby abandoned resort. Following him there, Suzume discovers a free-standing door, which she opens to find a starlit field that she cannot enter. She trips over a cat statue on the floor, which turns into a real cat and flees, before rushing to school.
During lunch, Suzume notices a large column of smoke outside the classroom window from the abandoned resort, which no one else can see. There, she finds the man from earlier struggling to close the door from which the smoke escapes. Suzume helps him lock the door with an old key. The smoke disappears, but not before causing earthquake-like damage to the town.
Suzume takes the injured man, Souta Munakata, to her home who reveals himself as a "Closer" who locates and locks specific doors in abandoned places throughout Japan to prevent a supernatural "worm" from being released, causing earthquakes. The cat from the resort turns Souta into the chair he was sitting on. He and Suzume chase the cat onto a ferry headed for Ehime. Souta tells Suzume that the cat is a "keystone" she removed at the resort, releasing the worm from it.
Upon reaching Ehime, Suzume and Souta find that netizens have dubbed the cat "Daijin". They encounter the worm again after helping a girl named Chika save oranges from rolling down a hill, with whom they travel to seal a door at an abandoned school. Afterwards, Suzume stays the night at Chika's family hotel.
The next day, Suzume and Souta hitchhike to Kobe with a woman named Rumi. Suzume helps at Rumi's bar before seeing Daijin leading them to an abandoned amusement park, stopping the worm from emerging through a ferris wheel gondola. While closing the door, Suzume asks about the starry field. Souta explains that the portal within the doors lead to the Ever-After, where souls go after death.
Tracking Daijin to Tokyo, Souta asks Suzume to take them to his apartment. He explains the legend of the worm, and that he is the last descendant of a generational family who locked doors to the Ever-After. The western keystone has become Daijin, while the location of the eastern keystone is unknown. He warns that if the worm tries to emerge in Tokyo, its damage will be similar to the 1923 Great Kantō earthquake.
Suzume notices the worm's emergence, so she and Souta hop in the worm as it fully breaks to find Daijin, who reveals that he has passed on his function as keystone to Souta and if they don't want the worm to fall, Souta has to be used to seal it. Souta suddenly starts crystalizing, forcing Suzume to use him to seal the worm.
Awakening at a shrine housing the Tokyo door, Suzume sees Souta within the Ever-After but is unable to enter. Suzume goes to visit Souta's grandfather Hitsujirō at the hospital, hoping to discover how to rescue Souta. Hitsujirō explains that Suzume's ability to see the worm and the Ever-After through the doors means that at some point in her life she entered the realm through one such door, the only door where she can re-enter the Ever-After.
Suzume runs into Souta's friend Tomoya Serizawa, and Tamaki, who wants to take her back home to Kyushu. She instead convinces Tomoya to drive her and Tamaki to her childhood hometown in Tōhoku, destroyed by the 2011 earthquake and tsunami that killed her mother, to find the door she first visited. At a rest stop along the way, Suzume discovers that her aunt is possessed by Sadaijin, the eastern keystone. They reach the ruins of Suzume's old house and town, after looking at her old journal from when she was a kid. Suzume finds the door and enters it with Daijin and Sadaijin.
Inside the Ever-After, Sadaijin distracts the worm, while Suzume awakens Souta, who regains his human form. Realizing the consequences of his freedom, Daijin reverts himself to being the western keystone. Suzume and Souta use him and Sadaijin to imprison the worm again in the Ever-After. Afterwards, Suzume sees a young girl in the Ever-After with them. She realizes the young girl is herself, from 12 years ago, and that the younger Suzume mistook her older self as her mother. Suzume gives her the chair that had been Souta's body, built by her mother as a childhood birthday present, allowing younger Suzume to leave the Ever-After, to be taken in by Tamaki. Souta returns to Tokyo while Suzume and Tamaki return to Kyushu. A year later, Suzume unexpectedly encounters Souta again at where they first met.