Fear learning is an adaptive, evolutionarily conserved process that allows us to respond appropriately to threats in the environment. These threats can vary across different contexts (e.g., a lion in your yard versus a lion in a zoo) and by age (e.g., a dentist viewed by a child before cavities versus by an adult after cavities). Using the high degree of neural and behavioral conservation across species in fear regulation and the underlying neural circuitry, we examined how fear learning changes across contexts and development, focusing specifically on the environmentally changing and challenging period of adolescence. We show two surprising developmental findings specific to adolescents relative to older and younger ages: 1) diminished fear to previously aversive contexts; and 2) heightened fear to previously aversive cues. These behavioral changes are paralleled by developmental changes in frontolimbic circuitry. We discuss how these evolutionarily conserved mechanisms may be essential to survival of the species with the changing environmental demands (social, sexual and physical) of adolescence. Our findings also have important implications for unremitting forms of fear at the very core of anxiety related disorders that peak during the period of adolescence and when, during development, specific treatments for these disorders may be most effective.