On a cool Michigan day in 1931, Robert Smith, a Black insurance agent, leaps from the roof of the local hospital wearing homemade wings imagining himself capable of flight. As he teeters on the precipice of death, people gather on the street below, horrified by the promise of the man's death. Among the crowd is Ruth Dead, who is so shocked by the sight of Robert plummeting to the earth that she goes into labor. 

In the chaos and confusion of Robert's death and Ruth's unexpected contractions, the young Black woman is admitted to the hospital. She delivers a boy, naming him Macon Dead III; he is the first Black child born in the hospital. 

As Macon grows, it is clear that, somehow, the somber events of his birth have influenced his life, as he is a quiet, disillusioned child who feels alienated from the outside world. His home life is complicated, and the Dead family is described as living "under the frozen heat of (their father's) glance." 

Moreover, his mother finds comfort in breastfeeding Macon, which she does until her son is four; their ritual is disrupted when a coworker of Macon's father accidentally walks in on Ruth breastfeeding the far-too-old Macon and jokingly nicknames him Milkman. However, Milkman's father, Macon Sr., refuses to call his son by this nickname and often treats him poorly. 

As time passes, readers learn more about the quiet desperation of the Dead household and the made-up town in which it sits. Ruth struggles with depression; nearly twenty years of an unhappy marriage and her husband's condescension have silenced her inner life and sense of self. The watermark on the dining room table she inherited from her father reminds her that she is a living being, conjuring memories of her happy childhood and her long-lost dreams; indeed, the watermark is the single, slim moor upon which Ruth preserves her sanity.

Macon Sr. works in real estate and makes his living as a landlord for the town's Black residents; he is an arrogant, selfish man whom they detest because of his similarity to the cruel white landlords who preceded him. Although those around Macon Sr. find him entirely unlikable, readers see that his internal life is complex and riddled with self-loathing; the only source of self-worth he has is his properties, which he finds pride in. When upset, he toys with the keys to the homes he owns to make himself feel better. 

The final character introduced in the first chapter is Pilate, Macon Sr.'s sister, who cared for Milkman when he was young. Macon Sr. warns his son from visiting Pilate, as he views his sister and her unusual perspective on life poorly and does not wish her to influence his son.

However, Milkman defies his father's wishes and visits Pilate at her remote house in the woods. As he peers through the woods at her home, he realizes that, to an extent, his father was right. Pilate is an odd woman. She was born without a navel, wears earrings with her name written inside them, and when Milkman first sees her, is singing with her family in the yard. Despite these unconventional traits, Milkman is mesmerized by Pilate and continues to visit her house quietly and without notice, captivated but unwilling to make himself known.