The story takes place on Pantala, a continent across the ocean from Pyrrhia, where three dragon tribes coexist under Queen Wasp's authoritarian rule. The HiveWings, who possess various natural weapons, dominate the other two tribes from massive city-structures called Hives. The SilkWings, gentle dragons who spin silk and undergo a metamorphosis to gain wings at age six, serve as laborers. The LeafWings, a green-scaled tribe with leaf-shaped wings, were believed wiped out during a conflict called the Tree Wars decades earlier.
The novel opens on Pyrrhia, where Moonwatcher (Moon), a NightWing who can read minds and see the future, sits on a beach with Luna, a SilkWing blown across the ocean from Pantala. Luna believes Moon is a second Clearsight, an ancient seer revered on Pantala, and expects her to help the Chrysalis, a secret SilkWing resistance group, defeat Queen Wasp. Moon shares a prophecy warning of a land where dragons are poisoned, with secrets hidden in eggs, a book, and underground. It declares the tribes must unite or none will survive. Moon's companion Qibli arrives with Turtle and Tsunami, siblings from the sea-dwelling SeaWing tribe, who reveal that Turtle's animus magic, a rare power to enchant objects, has stopped working. Tsunami proposes that she and Turtle swim to the lost continent instead.
The narrative shifts to Cricket, a young, bookish HiveWing. In a flashback to age two, Cricket witnesses her first whole-Hive command, in which Queen Wasp seizes control of every HiveWing simultaneously, turning their eyes white and speaking through their mouths. Cricket is horrified to see her older sister, Katydid, among the controlled mob but realizes she herself is unaffected. Katydid explains that the queen controls HiveWing bodies but cannot access their thoughts. For the next four years, Katydid helps Cricket conceal her immunity during Hive-mind events.
In the present, Cricket is a wanted fugitive. She has stolen the Book of Clearsight, an ancient text of prophecies that Queen Wasp uses to justify her rule, and helped flamesilk SilkWings, rare dragons who produce fire-generating silk, escape captivity. She waits in an underground cave beside the glowing cocoon of Blue, a kind SilkWing undergoing his Metamorphosis. Sundew, a fierce LeafWing, returns wounded from leading pursuers away and brings Blue's best friend Swordtail, whom she found unconscious after he tried to follow Luna out to sea.
Sundew reveals she wants Blue to use his flamesilk to burn down all the Hives. Cricket argues against this, pointing out that wingless SilkWing dragonets and their silk-connected homes would burn first. She redirects the conversation toward Queen Wasp as the real enemy, arguing that breaking her mind control would reveal which HiveWings might be allies. Swordtail mentions the Chrysalis may be researching the mind control. Sundew agrees to postpone violence but warns that her parents, the LeafWing leaders Belladonna and Hemlock, will not wait indefinitely.
After four days, Blue emerges from his cocoon and confirms he is a flamesilk. Sundew reveals her parents will wait only two more days before attacking. The group travels to Jewel Hive, ruled by Lady Jewel, Queen Wasp's cousin, whose chaotic culture will help them blend in. Cricket knows the Hive from visiting Cadelle, the dragon she believes to be her mother. They steal disguises from market stalls, hiding Sundew's LeafWing features, and find a hidden Chrysalis message at the base of the Salvation Statue.
The group hides near Cadelle's house, and Cricket spots Katydid sneaking inside. She rushes to speak with Katydid despite warnings from her friends. Katydid urges Cricket to turn herself in, dismissing Cricket's revelations about Queen Wasp's lies, and then reveals that Cadelle is not Cricket's mother and their father is not her father either. Before Katydid can explain, Lady Scarab, Lady Jewel's elderly mother and Queen Wasp's aunt, pounds on the door from her guard post outside.
At midnight, the group meets SilkWing Chrysalis members at the library, but the resistance has no useful information about the mind control. When HiveWing guards arrive, two members, Cinnabar and Tau, sacrifice themselves by pretending they broke in to read, protecting the others. The queen then receives a tip about Lady Scarab hiding someone.
Cricket watches as Scarab argues defiantly with Queen Wasp's soldiers, but Katydid steps out voluntarily to protect Scarab. The queen takes over Katydid's mind and marches her away. Cricket realizes Scarab, like herself, is immune to the mind control.
Visiting Scarab alone, Cricket learns that Clearsight married SilkWings and HiveWings descended from those unions, a fact omitted from official histories. Scarab reveals that Katydid is not Cricket's sister but her mother. Katydid had an egg with Malachite, Scarab's secretary, but Queen Wasp forbade the relationship to spite Scarab and took Malachite permanently into her Hive mind. Scarab helped Katydid and Cadelle, Cricket's grandmother, conceal the egg in the communal Nest under forged records.
Newly resolved, Cricket enlists her friends to copy Clearsight's final letter onto silk paper, adding messages exposing Queen Wasp's lies. To protect Blue and Sundew from capture, she distributes the messages alone, painting the truth across walls and the Salvation Statue throughout Jewel Hive. Her campaign ends when she encounters Cadelle, and Queen Wasp takes over Cadelle's mind to mobilize the Hive. Cricket is overwhelmed, paralyzed by stinger venom, and imprisoned in Lady Jewel's palace. The queen, speaking through guards, threatens to make Cricket controllable.
Lady Jewel visits Cricket with Scarab. Jewel reveals that the queen considers her a harmless fool, a perception Jewel exploits as cover. She confirms Queen Wasp can forcibly bring resistant dragons into her Hive mind, but the process fails on dragons with SilkWing ancestors in the last three generations. Cricket strikes a deal: Jewel will arrange her escape if Cricket infiltrates the Nest during the queen's scheduled inspection. Using flamesilk Jewel provides, Cricket escapes and hides in the Nest's rafters.
When Queen Wasp arrives, she reveals a hidden tail stinger and injects each egg with a bright green substance, marking each shell afterward. Cricket realizes this is how the mind control works: Wasp poisons dragonets before they hatch, linking them to her Hive mind from birth. Cricket deduces she escaped because Katydid smuggled her egg into the Nest after Wasp had already visited. She takes an unmarked orphan egg and flees through a storm.
Reuniting with her friends, Cricket shares everything. The orphan egg hatches, producing Bumblebee, an energetic dragonet who shows no signs of mind control, confirming Cricket's theory. Sundew examines green residue inside the shell and recognizes the smell: It comes from a plant filling Queen Wasp's private greenhouse near Wasp Hive.
The next morning, smoke rises from the south. Belladonna and the LeafWings have attacked Bloodworm Hive without waiting, though they warned the local Chrysalis to evacuate SilkWing dragonets first. With most HiveWings responding to the attack, the group sneaks into the queen's greenhouse. Sundew takes a cutting of the vine, hoping to find an antidote, and Blue uses his flamesilk to destroy the greenhouse and the queen's supply of the mind-control plant.
Sundew leads the group north toward the Poison Jungle, a deadly region where the LeafWings have hidden since the Tree Wars. Cricket, who has lost her home and family, carries hope in the form of Bumblebee and the vine cutting that may hold the key to freeing her tribe.
In a brief epilogue, Tsunami and Turtle swim into the Poison Jungle and are nearly killed by a giant snake before a LeafWing named Willow saves them. On the Pyrrhian beach, Moon tells Luna she has had a vision of burning cities on Pantala. When Luna asks if they have found a way to reach Pantala, Moon says they do not need to: The danger is coming to them.