The novel opens aboard a ship bound for Porttown, the capital of the Kingdom of Glaucus, where a merchant discovers his cabinmate dead, apparently poisoned. He picks the locks on the dead man's trunks and finds a brilliant silver, egg-shaped object in a wooden box inscribed with the Seal of Porttown. He pockets it and throws all accompanying papers overboard.
In Porttown, twelve-year-old Eva Alexander, the daughter of Arbor Alexander, a wealthy politician, and stepdaughter of the Duchess of Davenport, celebrates her birthday at the Young Ladies' Royal Academy for Science and Mathematics. At Bronsworth's Department Store, she spots the silver object and identifies its surface as rubibium, a rare explosive element. Intrigued, she insists on purchasing it.
In the Shambles, Porttown's poorest neighborhood, thirteen-year-old Dusty St. Ichabod lives in a workhouse. An orphan with a distinctive gray patch in his hair, Dusty has recently joined the Thieves' Union, a semi-secret criminal organization whose members bear a tattoo of five fish on their forearms. His closest friend, fifteen-year-old Calder "Cal" Ore, is the only person Dusty has known to survive the Kingdom's prolonged war against the Free Territories, a rebellious colony. Cal lost his left arm in combat and wears a bronze prosthetic.
Cal summons Dusty to a Union meeting where leaders explain that the silver object went missing from the ship and that Director Eoin Parnassus, head of the Department of Kingdom Secrets, killed a cabin boy in rage upon learning it was gone. Scouts trace the object to Eva, and Dusty is assigned to steal it because he already delivers milk to the Academy.
Eva and her roommate, Myrnie Wilshins, experiment with the object. It does not behave like rubibium: It catches fire without melting. Myrnie, an anxious ecology student with a condition called Advanced Social Hysteria that causes extreme panic in social situations, consults a book by Dr. Benedicta Frogg, a reclusive scientist who studies creatures dismissed as legendary. Myrnie identifies the object as an aerimander egg. Aerimanders are dragon-like winged lizards with wells of flame in their cores, once weaponized by a king who then ordered their total extinction, though Dr. Frogg argues they survived in hiding.
Parnassus, a sadistic official who plans to weaponize the egg against the Free Territories, visits the Academy to retrieve it. Eva hides the egg in a box of menstrual supplies and lies, saying she disposed of it. She resolves to take it to Dr. Frogg's cottage for safekeeping. Before the girls can leave, Dusty breaks into their room at dawn. Eva grabs the egg bare-handed to prevent him from taking it, and it fuses to her palm with searing pain. Unable to remove it, Dusty takes Eva with him, fleeing through the window.
Eva realizes she can exploit the situation: She was already heading into the forest, and Myrnie's coat, which Dusty grabbed by accident, contains a map to Dr. Frogg's cottage. During their trek, their relationship shifts from hostile to grudgingly conversational. Eva discovers Dusty cannot read and does not know what the egg is. When three members of the Kidnappers' Union, a criminal guild that specializes in abductions, ambush them in a cave, Eva plunges the egg into campfire smoke. It bursts into flame in her hand, but she feels only heat, not pain. She drives the kidnappers back while Dusty knocks two unconscious with his slingshot.
At the Lockwood Inn, a forest way station, Eva secretly arranges for sky poppy petals, a natural sedative, to be placed in Dusty's soup. He falls asleep, and she rides west toward Dr. Frogg's cottage. Dusty wakes and follows on a slow pony named Gourd. Alone in the woods after her horse bolts, Eva sits too close to her campfire and the egg nearly hatches. Peering into a widened crack, she glimpses a tiny reptilian eye, confirming the creature developing inside.
Myrnie escapes the Academy and reaches the Lockwood Inn, where she meets Cal. He claims to be a veteran searching for Eva, and they ride toward Dr. Frogg's together. At the cottage, the eccentric scientist confirms the egg is a female aerimander and applies a bitterroot salve to dissolve the bond with Eva's palm. Overnight, Eva discovers that Dr. Frogg has been stripped of her doctoral title and is desperate to restore her reputation. When the salve works the next morning, Dr. Frogg removes the egg and drops it into the fireplace, intending to hatch the aerimander to vindicate herself. Eva objects, and Dr. Frogg attacks her.
Dusty arrives, punches through the window, and grabs the egg bare-handed, fusing it to his own palm. An explosion destroys the cottage roof, and they escape on Gourd. On the road, the shell splits open and a tiny scarlet kit emerges, no bigger than a newborn kitten. She shakes sparks from her scales, showering Eva and Dusty with fire they feel only as warmth. Eva hypothesizes that fusing with the eggshell inoculated them against aerimander flame. They name the kit Rubi and resolve to take her to the Northern Isles, where wild herds may survive, rather than surrender her to Parnassus or the Union.
Myrnie and Cal arrive, but so does Parnassus with guardsmen. He addresses Cal by name, commending him. Parnassus tranquilizes Rubi, seizes her, and has Dusty bound. Cal takes Dusty's slingshot without meeting his eyes, and Dusty understands: Cal has been Parnassus's informant since the war, when Parnassus saved Cal's life in exchange for intelligence about the Union.
Eva and Myrnie are sent home; Dusty is imprisoned beneath City Hall. Parnassus visits Eva, revealing his plan to kill Dusty and pressing her for information about the Tricksters' Union, a rumored shadow organization embedded at every level of power. Eva knows nothing. In the dungeons, Dusty refuses Parnassus's fabricated offer of freedom in exchange for information.
Eva's father enrolls her at Byrdhaven, a remote reform school. Myrnie secretly gives her supplies: test tubes, wires, matches, and a map marking Porttown's royal manholes. On the ride to Byrdhaven, Eva detonates a homemade explosive, blowing open the locked carriage and a manhole cover. She descends underground, following the pull in her scarred hand toward Rubi.
She arrives as Cal attempts his own rescue, holding the sedated Rubi and threatening to wake her. Parnassus stabs Cal through the back. As Cal falls, his bronze prosthetic hand opens: He has already pulled the syringe. The aerimander wakes. Eva picks up Rubi, but when an agent draws a gun, the frightened kit unleashes a blast of flame that reduces the agent to ash. Cal is dead. Rubi bursts through the window and vanishes into the sky.
Eva and Dusty escape to the streets. On the docks, Eva says she must find Rubi. Dusty, devastated by Cal's death, presses his scarred palm against hers and walks away. He returns to St. Ichabod's to learn that Cal visited the boys the night Dusty disappeared, leaving a token they can use to get food and medicine from the Union. Dusty tells them to use it, says goodbye, and leaves.
Three weeks later, Eva endures Byrdhaven's bleak routine. She monitors the news and finds no further deaths reported, suggesting Rubi is alive. One evening, a rock strikes her window, then another. It did not come from a bird. It came from a slingshot. The novel ends with Eva recognizing that Dusty has come for her.