While empathy to the pain of conspecific is evolutionary-ancient and is observed in rodents and in primates, it also integrates higher-order affective representations. Yet, it is unclear whether human empathy for pain is inborn or matures during development and what neural processes underpin its maturation. Using magnetoencephalography, we monitored the brain response of children, adolescents, and adults (n = 209) to others' pain, testing the shift from childhood to adult functioning. Results indicate that children's vicarious empathy for pain operates via rudimentary sensory predictions involving alpha oscillations in somatosensory cortex, while adults' response recruits advanced mechanisms of updating sensory predictions and activating affective empathy in viceromotor cortex via higher-level representations involving beta- and gamma-band activity. Our findings suggest that full-blown empathy to others' pain emerges only in adulthood and involves a shift from sensory self-based to interoceptive other-focused mechanisms that support human altruism, maintain self-other differentiation, modulate feedback to monitor other's state, and activate a plan of action to alleviate other's suffering.