John Singer is the focal point of the other four main characters in The Heart Is a Lonely Hunter. Chapters narrated from Singer's point of view open the and close the first and second parts of the novel. McCullers's writing in these chapters is understated, simplistic, and largely expository, and the tone is calm. The deaf-mute Singer is a silver engraver at a local jewelry store; for ten years he has lived with his close friend Spiros Antonapoulos, another deaf-mute. Singer never seems to realize that he puts almost all of the effort into his friendship with Antonapoulos, but he is happy in this obliviousness. After Antonapoulos is taken away to an insane asylum at the end of Part One, Singer grows very sad and lonely and moves in as a boarder with the Kelly family.

Part Two of the novel chronicles the other characters' increasing dependence upon Singer. Each of them creates his or her own individual conception of who Singer is; because Singer himself cannot speak, he cannot refute or disillusion them. Singer demonstrates one of McCullers's main themes and one of her counter- themes, as he plays one role with Antonapoulos and another with the four other main characters. Singer's devotion to Antonapoulos is McCullers's means of exploring the human struggle to be loved and to express oneself. On the other hand, Singer is an object of such adoration and devotion from the other characters; in this sense he represents the counter-theme that any manmade god or object of worship is inevitably an illusion.