Eleven-year-old Masaru Saiga inherited a vast fortune after his father died in an accident. These riches make Masaru a target for kidnappers, who send fearsome puppets to abduct him. Masaru escapes with the help of circus employee Narumi Kato, but the kidnappers soon catch up with them. All seems lost until a mysterious woman named Shirogane appears.

After the briefest of respites, Masaru, Narumi and Shirogane are plunged into peril once more. Assassin Eiryo Ashihana has tracked them down and attacks with the evil clown-like marionette Pulcinella. Shirogane unleashes her own marionette Arlequin in response, but while she is distracted, Ashihana’s henchmen seize Masaru.

The kidnappers relentless attacks finally succeed and they snatch Masaru. Narumi and Shirogane discover that Masaru’s uncle, Zenji Saiga, is the mastermind behind the abduction, and they rush to his mansion to attempt a rescue. Masaru, meanwhile, tries to make his own escape, but in doing so stumbles across a shocking file written by his late father.

Masaru determines that overcoming his own weakness is the only way he will escape from his uncle Zenji. He comes face to face once more with his would-be assassin Ashihana, but chooses not to run and makes Ashihana a counter-offer to work for him instead. While attempting to rescue Masaru, Narumi and Shirogane are themselves captured by Zenji’s puppeteers and seem to have no way out...

After having rescued Masaru numerous times, Narumi got caught in the blast that destroyed Zenji’s mansion and has not been seen since. Masaru’s sense of loss is profound, but he is determined to be strong as Narumi had taught him. He decides to go back to school in an effort to return to a normal life. Shirogane also enrolls in the adjacent high school so she can continue to watch over Masaru.

Narumi, despite being presumed dead after the explosion in Karuizawa, awakens to find himself in a hospital. There he meets ladies' man Guy and an old woman named Lucille and struggles to regain his memory of what happened. As Narumi interacts with the hospital’s child patients and witnesses his own wounds healing with incredible speed, he begins to suspect that something strange is going on.

Having learned the truth about ZONAPHA syndrome, Narumi realizes there is only one way he can give children who suffer from it a chance of a future. He must destroy the automata the Midnight Circus uses to spread the disease. To do so he resolves to become a “shirogane” – a destroyer of automata. Meanwhile, Masaru and Shirogane have joined the Nakamachi Circus and encounter the mysterious Vilma.

With their numbers boosted by the addition of knife-thrower Vilma and their coffers swelled by successful fundraising, Nakamachi Circus are ready to put on a show in Izu. As they prepare for opening night, Narumi, Guy and Lucille board a plane for Shanghai on the trail of the Midnight Circus. However, several automata are also on board and a fierce fight breaks out high above the Pacific Ocean.

The members of Nakamachi Circus rescue the injured Guy, who turns out to be Shirogane’s marionette teacher. This unexpected reunion leads Shirogane to open up about her past to Masaru, who in turn sets out alone on a journey to solve the mysteries surrounding his own upbringing. Narumi also reunites with a figure from his past as he and Lucille meet his old martial arts master, Liang, in China.

Liang recounts the tale of the love triangle that lead to the birth of ZONAPHA syndrome. Brothers and aspiring alchemists Jin and Yin both fell in love with the same woman, Francine, and their rivalry unleashed the tragedy that would overtake the world. Narumi and his companions are still reacting to learning this terrible truth when Pantalone, one of the four oldest automata, appears before them.

The events in China allow the location of the Midnight Circus to be traced to the Sahara Desert. There, Narumi encounters desert-specialist Fatima, as shiroganes from around the world converge to annihilate the automata. Also gathering for the fight are the bionically enhanced shirogane-Os, led by Commander Faceless.

Inside the Midnight Circus’s big top, Narumi and his companions have managed to defeat Merry-Go-Round Olsen and the Acrobat Brothers. Presented with two doors, only one of which leads to Doll Francine, they decide to split into two groups. Beyond the doors, however, a new enemy lies in wait.

After fighting their way through to the center of the Midnight Circus’s big top, the shiroganes finally catch sight of Doll Francine. However, before they can reach her, they must first defeat the four oldest automata. When one of the four, Colombine, attempts to finish off the already gravely wounded Narumi, the other shiroganes find a new unity in their shared desire to protect him at all costs.

One life after another is extinguished in the fierce fighting. Narumi also teeters on the brink of death as Rockenfield attempts emergency surgery. Meanwhile, Arlequino and Pantalone regain their freedom after having been forbidden to move by Doll Francine’s exact lookalike, Doll Angelina. As the situation grows bleaker, Narumi opens his eyes, his body now infused with the hopes of his friends.

Masaru seeks birth answers, visits childhood home, recalls Saiga family, heads to Karakuri mansion to uncover mysteries.

Having set out alone to seek answers to the mysteries surrounding his birth, Masaru visits the apartment where he lived with his mother. There he remembers being taken in by the Saiga family after her death, but can't seem to remember his father Sadayoshi's face. As his thoughts turn to conversations with his grandfather Shoji, Masaru then heads for the place he was reborn, the Karakuri mansion.

Masaru has been captured by the Kuroga puppeteers. When he regains consciousness, he sees in front of him his grandfather Shoji, who Masaru had thought dead. However, the once kindly Shoji is now hostile and calls Masaru by his father’s name, Sadayoshi. Forced to drink Shoji’s Aqua Vitae-infused blood, Masaru begins to experience Shoji’s memories of working as a town doctor in Tempo-era Nagasaki.

Captured by Kuroga puppeteers, Masaru meets hostile grandfather Shoji, drinks his blood, experiences Shoji's Tempo-era Nagasaki memories.

Masaru continues to journey through Shoji’s memories. Therein he sees Shoji drink the Aqua Vitae and decide to live with Angelina. With her by his side, Shoji devotes himself to developing marionettes to aid the shiroganes. The couple are then visited by a man named Dean Maistre, who has traveled from France on Lucille's orders to help supply Shoji’s marionettes to shiroganes around the world.

Shoji and Angelina’s daughter Éléonore comes into the world. Her birth is the catalyst for a gradual change in the attitudes of Guy and Doll Francine. However, the sense of happiness that pervades the group proves fleeting, as eerie mechanical sounds signal an assault on Kuroga village by the automata.

Masaru escapes captors, meets Shirogane. Pursued, he envisions Éléonore drinking Aqua Vitae, breaking Angelina's hopes.

After regaining consciousness, Masaru manages to escape from his captors and resolves to prove he is not Sadayoshi. Pursued by Guy and the Kuroga clan, he unexpectedly runs into Shirogane, who had come to Kuroga looking for him. However, before they can get away, another vision floods Masaru’s mind. In the vision, Angelina’s hopes have been dashed as Éléonore has ended up drinking the Aqua Vitae.

Sadayoshi intended to bond Masaru with Éléonore via data. Shoji thinks Masaru is Sadayoshi, but Kuroga member reveals hidden truth.

To download his brain’s data into Masaru and thereby form an intimate bond with Éléonore. That was Sadayoshi’s intent. Despite Masaru’s tears at seeing so many people’s hopes crushed within Shoji’s memories, Shoji and Guy remain convinced he is Sadayoshi. Just as Guy is about to turn his knife on Masaru, one of the Kuroga clan unexpectedly interrupts to reveal a truth of which not even Shoji knew.