Gaze following, or co-orienting with others, is a foundational skill for human social behavior. The emergence of this capacity scaffolds critical human-specific abilities such as theory of mind and language. Nonhuman primates also follow others’ gaze, but less is known about how the cognitive mechanisms supporting this behavior develop over the lifespan. Here we experimentally tested gaze following in 481 semi-free-ranging rhesus macaques (Macaca mulatta) ranging from infancy to old age. We found that monkeys began to follow gaze in infancy and this response peaked in the juvenile period—suggesting that younger monkeys were especially attuned to gaze information, like humans. After sexual maturity, monkeys exhibited human-like sex-differences in gaze following, with adult females showing more gaze following than males. Finally, older monkeys showed reduced propensity to follow gaze, just as older humans do. In a second study (n=80), we confirmed that macaques exhibit similar baseline rates of looking upwards in a control condition, regardless of age. Our findings indicate that—despite important differences in human and nonhuman primate life history characteristics and typical social experiences—monkeys undergo robust ontogenetic shifts in gaze following across early development, adulthood, and aging that are strikingly similar to those of humans.