Robert Smith, an insurance agent in an unnamed Michigan town, leaps off the roof of Mercy Hospital wearing blue silk wings and claiming that he will fly to the opposite shore of Lake Superior. Mr. Smith plummets to his death. The next day, Ruth Foster Dead, the daughter of the first Black doctor in town, gives birth to the first Black child born in Mercy Hospital, Milkman Dead.

Discovering at age four that humans cannot fly, young Milkman loses all interest in himself and others. He grows up nourished by the love of his mother and his aunt, Pilate. He is taken care of by his sisters, First Corinthians and Magdalene (called Lena), and adored by his lover and cousin, Hagar. Milkman does not reciprocate their kindness and grows up bored and privileged. In his lack of compassion, Milkman resembles his father, Macon Dead II (Macon Jr.), a ruthless landlord who pursues only the accumulation of wealth.

Milkman is afflicted with a genetic malady, an emotional disease that has its origins in oppressions endured by past generations and passed on to future ones. Milkman’s grandfather, Macon Dead, received his odd name when a drunk Union soldier erroneously filled out his documents (his grandfather’s given name remains unknown to Milkman). Eventually, Macon was killed while defending his land. His two children, Macon Jr. and Pilate, were irreversibly scarred by witnessing the murder and became estranged from each other. Pilate has become a poor but strong and independent woman, the mother of a family that includes her daughter, Reba, and her granddaughter, Hagar. In contrast, Macon Jr. spends his time acquiring wealth. Both his family and his tenants revile him.

By the time Milkman reaches the age of thirty-two, he feels stifled living with his parents and wants to escape to somewhere else. Macon Jr. informs Milkman that Pilate may have millions of dollars in gold wrapped in a green tarp suspended from the ceiling of her rundown shack. With the help of his best friend, Guitar Bains, whom he promises a share of the loot, Milkman robs Pilate. Inside the green tarp, Milkman and Guitar find only some rocks and a human skeleton. We later learn that the skeleton is that of Milkman’s grandfather, Macon Dead I. Guitar is especially disappointed not to find the gold because he needs the funds to carry out his mission for the Seven Days, a secret society that avenges injustices committed against African-Americans by murdering innocent whites.

Thinking that the gold might be in a cave near Macon’s old Pennsylvania farm, Milkman leaves his hometown in Michigan and heads south, promising Guitar a share of whatever gold he finds. Before he leaves, Milkman severs his romantic relationship with Hagar, who is driven mad by his rejection and tries to kill Milkman on multiple occasions. After arriving in Montour County, Pennsylvania, Milkman discovers that there is no gold to be found. He looks for his long-lost family history rather than for gold. Milkman meets Circe, an old midwife who helped deliver Macon Jr. and Pilate. Circe tells Milkman that Macon’s original name was Jake and that he was married to an Indian girl, Sing.

Encouraged by his findings, Milkman heads south to Shalimar, his grandfather’s ancestral home in Virginia. Milkman does not know that he is being followed by Guitar, who wants to murder Milkman because he believes that Milkman has cheated him out of his share of the gold. While Milkman initially feels uncomfortable in Shalimar’s small-town atmosphere, he grows to love it as he uncovers more and more clues about his family history. Milkman finds that Jake’s father, his great-grandfather, was the legendary flying African, Solomon, who escaped slavery by flying back to Africa. Although Solomon’s flight was miraculous, it left a scar on his family that has lasted for generations. After an unsuccessful attempt to take Jake, his youngest son, with him on the flight, Solomon abandoned his wife, Ryna, and their twenty-one children. Unable to cope without a husband, Ryna went insane, leaving Jake to be raised by Heddy, an Indian woman whose daughter, Sing, he married.

Milkman’s findings give him profound joy and a sense of purpose. Milkman becomes a compassionate, responsible adult. After surviving an assassination attempt at Guitar’s hands, Milkman returns home to Michigan to tell Macon Jr. and Pilate about his discoveries. At home, he finds that Hagar has died of a broken heart and that the emotional problems plaguing his family have not gone away. Nevertheless, Milkman accompanies Pilate back to Shalimar, where they bury Jake’s bones on Solomon’s Leap, the mountain from which Solomon’s flight to Africa began. Immediately after Jake’s burial, Pilate is struck dead by a bullet that Guitar had intended for Milkman. Heartbroken over Pilate’s death but invigorated by his recent transformation, Milkman calls out Guitar’s name and leaps toward him.