Elucidating the socio-ecological factors that shape patterns of aging in long-lived vertebrates is of broad interest to evolutionary biologists, geroscientists, and ecologists. However, research on aging in wild populations still faces challenges due to the difficulty of measuring cellular hallmarks of aging non-invasively and the difficulty of accurately estimating age in long-lived species. Here, we demonstrate that cellular DNA methylation (DNAm) profiles from faecal samples provide an accurate and reliable molecular clock for the estimation of age in a population of wild capuchins, a non-human primate species with exceptional longevity. Analysis of blood, faeces, and urine samples from a closely related species shows that DNAm differentiates between species and different types of biological samples, validating their biological specificity. We further find age-associated differences in DNAm relevant to development, membrane excitability, and control of the cell cycle. By generating new data on molecular aging in a long-lived, socially complex primate and demonstrating that DNAm can be studied non-invasively in wild animals, our research opens up new avenues for studying the socioecological determinants of aging and increases the potential for cross-population and cross-species comparisons.