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.