Elegant has been murdered, and his corpse lies undiscovered at the bottom of a well. Speaking from the afterlife, he hopes that his body is found soon and that the murderer is captured. Meanwhile, Black has returned to Istanbul after 12 years away. Before he left, Black fell in love with his cousin, Shekure, and he has now been summoned home by Shekure’s father (and Black’s uncle) Enishte. Enishte wants Black to work on a secret book commissioned by the Sultan and illustrated by the three master miniaturists, Butterfly, Stork, and Olive.
The murderer reflects on his difficulty coming to terms with the fact that he has taken someone’s life. He has started frequenting a coffeehouse where a storyteller entertains the audience by impersonating different characters; the murderer laughs at the storyteller’s impression of a dog, and he admits that he killed Elegant because Elegant was threatening to tell everyone about the secret book.
Enishte originally sent Black away after learning that he had fallen in love with Shekure, but he is now pleased with the way that Black has matured during his time in exile. He tells Black about a trip he took to Venice, during which he was astonished (and frightened) by the new realist style of European painting. Enishte introduces Black to Shekure’s six-year-old son Orhan, who then overhears Enishte telling Black about the death of Elegant, whom people suspect was murdered. As Black leaves Enishte’s house, Esther, a Jewish clothier, gives him a letter from Shekure. Riding away on his horse, Black catches a glimpse of Shekure at her window. Shekure admires Black’s handsomeness, but feels conflicted, as she is still technically married to a soldier who never returned from war. Shekure previously lived with her husband’s father and his brother, Hasan, but left when Hasan tried to rape her.
The next chapter is narrated by an illustration of a tree, who declares that it is lonely because it fell out of the book of which it was supposed to be a part. Meanwhile, Black goes to see Master Osman, the Head Illuminator, and he is given a tour of the Royal Workshop. Osman is suspicious of Black, as Enishte is Osman’s archrival. Black then makes individual visits to Butterfly, Stork, and Olive, who each tell Black three different parables about style and signature.
Black gives Esther a letter for Shekure, but before bringing it to Shekure, Esther shows it to Hasan, who writes his own letter. After receiving both letters, Shekure confesses that she is confused about whom to marry. Enishte goes to Elegant’s funeral, where Butterfly tells him that he believes Olive and Stork are behind Elegant’s death. The murderer admits that he put on a big show of grief at the funeral and that he does feel a genuine sense of torment about killing Elegant.
The storyteller’s next narrative is told from the perspective of a gold counterfeit coin, who argues that the people of Istanbul are all obsessed with money. Enishte explains to Black that the final illustration in the secret book will be a portrait of the Sultan, although Enishte is having trouble finishing it. The murderer sees Black leaving Enishte’s house and realizes that Black intends to marry Shekure, which fills the murderer with furious jealousy.
After Esther shows Hasan more letters between Black and Shekure, Hasan writes his own letter to Shekure, threatening to force her to return to his father’s house. Shekure and Black meet at a house that formerly belonged to a Jewish man who was hanged. They kiss and begin to have sex, but Shekure insists that they stop and she makes Black agree to a list of demands in preparation for their marriage.
While Shekure and Black are out, the murderer goes to Enishte’s house and they have a long conversation about art, religion, sin, and the secret book. Eventually, the murderer tells Enishte that it was he who murdered Elegant. They continue their discussion, but it becomes clear to both of them that the murderer intends to kill Enishte. The murderer smashes a Mongolian inkpot over Enishte’s head, and Enishte cries out in agony before dying. His soul is carried to the heavens in the palm of the Angel Azrael.
Shekure walks home in the snow, discovers Enishte’s dead body, and hides the body while pretending to her two sons that Enishte is merely sick. At the coffeehouse, the storyteller speaks from the perspective of the color red, reflecting on the impossibility of explaining color to someone who has never seen it.
In the morning, Shekure meets Black and makes a plan to legally authorize her widowhood so that they can marry. Black bribes an imam to issue the certificate of widowhood and arranges for the imam to officiate their marriage. The wedding takes place around Enishte’s body, with Shekure and Black managing to convince the imam and guests that Enishte is alive and providing his consent from his deathbed. That night, Hasan comes to Enishte’s house and threatens to force Shekure to come back to his father’s house. In the morning, Shekure tells the children that Enishte has just died; her eldest son, Shevket, doesn’t believe her, claiming that he knows Enishte died the previous night.
Black goes to the palace to bring news of Enishte’s death to the Sultan, who is deeply saddened. Black explains that the murderer stole the final illustration for the book, adding that Enishte believed that Elegant was murdered by one of the three master miniaturists and that Enishte’s and Elegant’s murderer is likely the same person.
Enishte is pleased by his funeral, which he witnesses from the afterlife. He explains that after dying he experienced a dazzling array of vivid colors, a collapse of time and space into a single plane, and a conversation in which Allah reassured him about his use of the European style, stating: “East and West belong to me.” After Enishte’s funeral, Esther visits Elegant’s widow, Kabilye, who shows her a drawing of horses that was found on Elegant’s dead body. Kabilye insists that Elegant did not create the drawing himself.
Black is summoned to the palace, where his head is put in a vice. However, just as the torture begins Master Osman interrupts and explains that the Sultan has given them three days in which to figure out who killed Enishte. Black and Osman discuss the particular characteristics of each of the miniaturists, and Osman states that he believes Stork is the murderer. One of the palace officials shows them the horse illustration found on Elegant’s dead body, and they resolve to hold a pretend horse-drawing competition in order to figure out which miniaturist drew the horses, and thus which one is the murderer.
Olive, Butterfly, and Stork each draw horses for the competition, and the murderer asks the reader if they were able to identify him through his drawing. He then describes going to the coffeehouse, where he tells two stories. As he is about to tell a third, he is cut off by the storyteller, who impersonates Satan and claims that evil and free will are important parts of the world and that Allah does not care about minor sins.
Having reached a dead end with the competition, Black goes to the palace, where Master Osman obtains the Sultan’s permission to look through the Royal Treasury for clues that will lead to the murderer. Black and Osman spend hours searching through the books in the treasury and having occasional conversations about the history and future of the miniaturist tradition. Eventually, Black falls asleep, and Master Osman happens upon the needle that Bihzad used both to paint and, eventually, to blind himself. Osman pierces his own eyes with the same needle, and his vision begins to slip away.
When Black is awake again, he and Osman discuss the identity of the murderer; Osman insists that it is Stork. Black goes home in a joyful mood, but he finds that Shekure and the boys are not there. He learns that they are at Hasan’s house and he brings a gang of men from the neighborhood to help him take Shekure back. After some confusion, Hasan’s father permits Shekure and the children to leave. At this moment, the Erzurumis descend on the coffeehouse; Black sends Shekure home and promises to join her soon.
At the coffeehouse, the storyteller tells of his desire to be a woman and he sings a poem about conflicted identity. When the Erzurumis raid the coffeehouse, they kill the storyteller, and Black and Butterfly go to Butterfly’s house. Black interrogates Butterfly and Butterfly pins him to the ground in an aggressive, erotic gesture. Butterfly says he believes Stork is the murderer, and he and Black set off for Stork’s house.
Once there, Stork tells them that Olive drew the horse illustration found on Enishte’s dead body. He adds that Olive will be at the abandoned dervish lodge, which is indeed where they find him. Olive denies drawing the horses. Stork and Black search for the book’s final illustration but find nothing. Olive begins to cry, and it is now clear to everyone present that he is the murderer. He suggests that the miniaturists must now kill Master Osman, and Black puts a knife to Olive’s throat, demanding to know the location of the final illustration. There is a scuffle during which the murderer is blinded. He confesses to both murders and tells the others that there is only once chance to escape the death of the miniaturist tradition—move to India, where the Sultan of Hindustan is gathering the best miniaturists for his royal workshop.
Olive attempts to kill Black but he misses, and then he runs away through the streets of Istanbul and encounters Hasan, who—mistaking Olive for one of Black’s allies—cuts off his head.
In the final chapter, Shekure tells of the fates of the characters after the main narrative ends. She explains that she told the story to Orhan and showed him the letters she exchanged with Hasan and Black, warning the reader that Orhan may not tell the exact truth but that this is in service of creating “a delightful and convincing story.”