All of Part Three takes place in the space of a single day—August 21, 1939. Chapter 1 is narrated through Dr. Copeland's point of view, and takes place in the morning. Portia and the rest of the Doctor's family have decided that he should go to live with Grandpapa on the farm so that he can get well. Most of Dr. Copeland's furniture is moved to Portia's house, and a few things are strapped on the automobile.
Dr. Copeland is very bitter about the move and about his situation in general. He does not feel that his work is done and he does not want to leave. He thinks about John Singer's death, which makes him terribly sad. Then Dr. Copeland thinks again of the plight of his people, and he can feel the love and wrath swell simultaneously and make him feel sick. He feels defeated and alone as he rides away in the wagon.
Chapter 2 is narrated through Jake Blount's point of view, in the afternoon of the same day. A terrible fight has just erupted at the carnival, but rather than having tried to restore order, Jake had blindly started fighting, hitting both black people and white people. He had fallen down as the fight was dying down and had realized he was lying next to the dead body of Lancy Davis, who had been killed in the fight.
Jake runs from the carnival grounds, goes home, and packs all his possessions. He tries to find Dr. Copeland to make amends with him. but Portia informs him that the Doctor has left. Jake gets caught in a downpour and goes to the New York Café. He talks with Biff Brannon for a while, who gives him a free meal. Blount falls asleep briefly and has a nightmare in which he is walking through a crowd carrying a covered box and does not know where to put it down. Biff wakes Jake up and gives him forty dollars before he leaves. Jake thanks Biff and heads for the train station, uncertain of his destination.
Chapter 3 is told through Mick's eyes, on the evening of the same day. Mick is wondering what good all of her plans are now that all she has time to do is work every day. On this day she has had to work overtime at Woolworth's. When her shift ends she goes to the New York Café and orders a chocolate sundae and a beer. She reflects that there are two aspects of her life that she cannot believe: that she is working at Woolworth's and is all grown up, and that Mr. Singer is dead.
As Mick drinks her beer and eats her sundae, she reflects that she is locked out of the "inside room" all the time now; however, she cannot tell if this is because her job makes her tired or because her job makes her tense. Then, Mick thinks of her plans to set aside money to pay off the rest of the installments on Singer's radio and to buy a little piano. She is determined that she will pursue her plans.
Chapter 4 is told through Biff Brannon's point of view, late at night on the same day. He arranges some zinnias for the flower display in the front window, and when he is finished he decides that his work looks very artistic. He ponders why he keeps the café open all night, because between midnight and five in the morning there are hardly any customers. Biff decides the reason he keeps the restaurant open is that the night is restful and meditative, and he likes to be awake during these hours.
Biff thinks about the women he has loved in the past and about the strange love he felt for Mick over the past year. This love has faded for Biff after Singer's death. Biff ponders Singer's suicide and thinks that it is another riddle he must ponder. At the end of the novel, as Biff looks into a mirror, he has a fleeting epiphany about the human condition. Then he turns away, and readies himself to greet the approaching day.
Part Three serves as a sort of coda to the musical composition that is The Heart Is a Lonely Hunter, as the continuing struggles of the four remaining main characters are played out. At the time McCullers outlined her novel, she assumed that John Singer—the character to whom the other four characters would relate—would perplex them until his suicide at the end of Part Two. However, she had planned that upon Singer's death, the other characters would begin to understand him, and, by extension, would begin to understand themselves and each other. However, Singer's death does not end up elucidating anything for anyone; in fact, he baffles the other characters more in death than he has done in life. Because Singer's life is mysterious, it allows each person to create or define Singer as they wish him to exist. His suicide does not harmonize with anyone's previous conception of him. Because Singer is locked into a world of silence, he is essentially a static character in the novel. He does not respond to the other characters, and he remains remote from them and uncomplicated in his life and in his love for one other person, Antonapoulos. Only through each character's romantic idealization of Singer does he gain complexity. Because his suicide neither enhances the four individuals' self-understanding nor draws them together in any way, the integration of themes for a dramatic finale does not happen as McCullers had planned. Each character experiences his or her bewilderment and grief alone.
Indeed, none of the characters appears able to reconcile Singer's death with his or her everyday life or with all the private dreams and aspirations he or she confided in him. Dr. Copeland is saddened and confused that such a just man would choose to take his own life. Jake Blount is angered that he put all his stock in a man who is now dead, so he leaves town. Mick continues on with her job, determined to save money to pursue her musical ambitions. Biff continues working at the café, spending the quiet of the late night musing on his scattered thoughts and observations. Biff's momentary epiphany at the very end of the novel appears to reveal to him that human love and labor—however misguided and in whatever form—are the only two ideas that give meaning to life. Biff's is the only insight that is uplifting and different than anything we have seen before; the other characters simply proceed with life as usual, without reaching any sort of new outlook or change in direction.
McCullers used musical terms to describe the style of her projected novel as a contrapuntal work. Each character would be one voice in a fugue, a voice complete in itself but also enriched by the contrast and interweaving with the other voices in the story. The contrapuntal effect would arise from McCullers's effort to give a distinct style to the narratives of each of the four characters who seek Singer's support. A fifth style, legend-like in tone and parable-like in simplicity, would represent Singer. Indeed, McCullers achieves a remarkable range of dialogue, pace, and tone in The Heart Is a Lonely Hunter; thoughts and feelings emerge almost entirely through explicit action and direct dialogue.