Biff Brannon is one of the more bizarre characters in the novel. Like Singer, he is distanced, observant, and quiet. However, none of Biff's observations cohere into any greater insight or concept of humanity; instead, they stand as isolated, unconnected fragments that offer us only puzzling and contradictory impulses that are never satisfactorily explained. When we sees Biff interact with his wife, Alice, at the beginning of the novel, it is clear that the two do not feel any great love for one another after fifteen years of marriage. We also learn that Biff is impotent, though we are never told if this condition is just a problem he has in his relations with Alice or whether it extends to other women as well. Throughout The Heart is a Lonely Hunter, we perceive that Biff also has a strong desire to have children of his own; he wishes that Mick and his niece, Baby, were his own children.

Biff clearly has unresolved sexual anxieties, but their exact nature is never made clear. He keeps all the parts of his life compartmentalized—the past from the present, his life upstairs in his room from his life downstairs in the restaurant, and his marital relationship from his sexual life. At one point, we learn that Biff chivalrously beat up his sister-in-law's husband when he bragged about beating her; yet after Alice dies, Biff starts to sew and use his wife's perfume, expressing an unexpected feminine side to his personality. Neither Biff nor McCullers explains or integrates these conflicting impulses, which leaves us to assume that Biff himself is unable to resolve these inner conflicts.

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