As the film opens, we are taken back by a heartfelt flashback to a serene field where a young Suzume Iwato wanders alone, her voice echoing as she calls out for her mother. This touching moment is brightened by a gentle smile, and as Suzume's tears fade, we shift to her older self who awakens from this poignant dream.
Now a teenager living with her aunt Tamaki Iwato in Kyushu, Suzume's daily life takes an unexpected turn when she encounters Sota Munakata, who ignites a familiar spark within her. While she navigates the trials of high school, the memory of this mysterious stranger lingers in her mind, drawing her further into an intriguing journey.
Driven by her curiosity, Suzume seeks answers at an abandoned onsen resort, where she discovers a door leading to a mesmerizing starry realm known as the Ever-After. Despite her initial inability to enter this magical space, her determination to uncover its mysteries compels her to try further.
Her adventure escalates when she comes across a frozen cat statue, which, upon thawing, transforms into a living feline that quickly vanishes, leaving Suzume pondering the meaning behind this encounter. Suddenly, an earthquake’s tremors break her reverie, and a swirling vortex manifests, revealing chaos only Suzume can see.
In the midst of this turmoil, she finds herself back at the onsen, where Sota battles an entity known as "The Worm." With his mentorship, Suzume aids him in sealing away this malevolent force, which erupts in a deluge of rain as a result.
After the turmoil, Suzume cares for Sota, tending to his injuries while learning that he is a "closer," a protector of the Earth against the Worm's devastating influence. The mysterious cat reappears at her window, its likeable demeanor revealing a surprising connection to Suzume. However, its attention shifts to Sota, and with intense resolve, the cat morphs him into a three-legged chair—a bizarre twist that irrevocably links him to her life.
As the chase for the feline named Daijin intensifies, they end up on a boat, which Daijin hijacks toward the Ehime Ferry. Meanwhile, social media explodes with tales regarding the unusual running chair, dubbed "Daijin," highlighting its crucial role in warding off the Worm. Suzume and Sota soon realize that removing Daijin had unleashed dark forces upon them.
Their quest leads them to meet Chika Amabe, an exuberant young girl who, after a mishap with her oranges, inspires Suzume and Sota to lend a helping hand. In their continued mission, they encounter the Worm once again through another door in Shikoku. Sota explains to Suzume that to close this portal, she must delve into the collective memories of the area’s past inhabitants. Through this journey of empathy, Suzume unlocks those secrets, enabling them to secure the doorway.
After a heartfelt goodbye to Chika, Suzume and Sota remain focused on finding Daijin. They soon wind up at the home of Rumi Ninomiya, a caring woman whose children mistake Sota for a sophisticated toy robot. While Suzume assists Rumi, the pair catch sight of Daijin once more, prompting them to pursue once again.
Their relentless pursuit brings them to a derelict amusement park, where an eerie portal pulsates with energy, necessitating sealing to thwart further chaos. A climactic confrontation at the Ferris wheel results in a desperate attempt to reverse Sota's transformation into a chair, leading to a tumble from their precarious spot, and ultimately, a return to Rumi’s home for respite.
Later, navigating in Tokyo, Sota reveals the ancient legend of Namazu—the formidable Worm that could devastate the city if unleashed. Meanwhile, unexpected news from Tomoya Serizawa about Sota's personal struggles deepens their perilous situation.
As they venture out again, the sight of Daijin looming at the Tokyo gate creates an air of dread. Awareness dawns that the Worm is on the brink of escaping, intensifying their race against time. Daijin reveals he has made Sota the keystone in this impending disaster, intertwining their fates; it becomes clear to Suzume that she must embrace her new role with urgency.
With Sota firmly established as the keystone, Suzume places him upon the Worm, sealing the gateway and sacrificing any chance of altering his destiny. Daijin's sorrow is evident as Suzume bids him farewell, each word laden with emotion.
Following this pivotal juncture, Suzume is drawn to Sota's grandfather, Hitsujiro, in the hospital, where he shares his knowledge of the Worm and its gates, hinting at a deeper connection that may offer hope. Hitsujiro suggests that if Suzume can reach the Ever-After, she might have the means to save Sota.
As she departs, Tamaki, in a frantic search, finally finds her. Joined by Serizawa, they set off to locate Sota, leading to revelations and tensions reflecting on Tamaki’s actions being manipulated by a dark force, Sadaijin, that takes form as a menacing black cat.
Arriving at Tamaki's childhood home—a haunting site steeped in tragedy—Suzume uncovers a doorway leading to the Ever-After, where both Daijin and Sadaijin dwell. With the Worm threatening to break free, Sadaijin takes battle form against this evil, while Suzume discovers Sota ensnared in chair-like confinement.
Ultimately, Daijin embraces his fate as a keystone, enabling Sota to regain his humanity, but only after beseeching Suzume to restore his original position. With Daijin’s sacrifice, the Worm is defeated, and the Ever-After sealed away.
As Suzume gazes upon the horizon, she is transported back to her younger self, now grieving her mother. The older Suzume comforts her, promising brighter days ahead filled with love alongside Sota. She gifts her younger self the cherished chair crafted by her mother’s care.
As they part ways, Sota returns to his duties as a closer, promising to reunite with Suzume. The young woman rediscovers connections with Tamaki, introducing her to Rumi and embracing her academic dreams while cherishing the serendipitous meetings with Chika, reinforcing that Sota's return—bringing closure and joy—will illuminate her journey ahead.
