Evolutionary theories of aging are linked to life-history theory in that age-specific schedules of reproduction and survival determine the trajectory of age-specific mutation/selection balances across the life span and thus the rate of senescence. This is predicted to manifest at the organismal level in the evolution of energy allocation strategies of investing in somatic maintenance and robust stress responses in less hazardous environments in exchange for energy spent on growth and reproduction. Here we report experiments from long-studied populations of western terrestrial garter snakes (Thamnophis elegans) that reside in low and high extrinsic mortality environments, with evolved long and short life spans, respectively. Laboratory common-environment colonies of these two ecotypes were tested for a suite of physiological traits after control and stressed gestations. In offspring derived from control and corticosterone-treated dams, we measured resting metabolism; mitochondrial oxygen consumption, ATP and free radical production rates; and erythrocyte DNA damage and repair ability. We evaluated whether these aging biomarkers mirrored the evolution of life span and whether they were sensitive to stress. Neonates from the long-lived ecotype (1) were smaller, (2) consumed equal amounts of oxygen when corrected for body mass, (3) had DNA that damaged more readily but repaired more efficiently, and (4) had more efficient mitochondria and more efficient cellular antioxidant defenses than short-lived snakes. Many ecotype differences were enhanced in offspring derived from stress-treated dams, which supports the conclusion that nongenetic maternal effects may further impact the cellular stress defenses of offspring. Our findings reveal that physiological evolution underpins reptilian life histories and sheds light on the connectedness between stress response and aging pathways in wild-dwelling organisms.