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Abstract Long‐term studies of plant and animal populations are rare, particularly for long‐lived species with slow life histories. However, such studies are necessary to understand how population dynamics are affected by variation in vital rates. We used a large capture–recapture dataset spanning four decades (1983–2019) to estimate several population parameters for adult females in a metapopulation of a long‐lived North American pitviper (timber rattlesnake, Crotalus horridus ) near the northern extent of the species' geographic range. Apparent survival (ϕ, hereafter; survival) estimates were variable (0.595–0.938) among years, but generally high, whereas the annual recruitment rate ( f ) was low (0.102, 95% CI: 0.088–0.117). Survival increased by a quadratic function of mean body mass of the adult female population, resulting in survival increasing with this temporally varying population‐level covariate until the population average reached approximately 768 g; thereafter, survival decreased with increasing mean mass. The proximate causes of decreased survival for the largest, and thus presumably oldest, snakes remain unknown but are likely related to senescence and increased predation risk with advancing age. The best predictors for encounter probabilities were the additive effects of color morph (higher for yellow‐morph snakes than black‐morph snakes), sampling site, and year. The model‐averaged estimate of realized population growth () was 0.992 (95% CI: 0.980–1.005), but removal of sampling variance from the component of contributed by survival resulted in a 95% upper limit of 0.9997, indicating a declining population. Reflecting attributes of the species' protracted life history (late maturation, low fecundity, and infrequent reproduction), the contribution of survival was on average 8.9 (95% CI: 7.6–10.4) times greater than the contribution of recruitment to , representing the slowest life history documented for any snake population to date. Our findings suggest that management efforts to increase adult survival, such as reducing mortality from anthropogenic factors, should aid in the conservation of timber rattlesnakes and other imperiled species with similar slow life histories.