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ABSTRACT Males of polygynous mammals often do not live as long as females and, in some cases, exhibit evidence of earlier senescence. Patterns of DNA methylation (DNAm) have recently been used to predict chronological age in mammals. Whether DNAm also changes as a consequence of survival and senescence is largely untested in wild animals. In this study, we estimate mortality rates using recaptures of 2700 greater spear‐nosed bats,Phyllostomus hastatus, over 34 years and DNAm profiled for over 300 adult bats. In this species, one male typically controls mating access to a group of unrelated females. Bayesian analysis reveals that mortality risk in males is 1.8 times that of females, and comparison of age‐associated differences in DNAm indicates that DNAm changes 1.4 times faster in males than females. Therefore, even though the age of either sex is predicted by a common set of sites, the methylome of males is more dynamic than that of females. Sites associated with sex differences in the rate of DNAm change are sensitive to androgens and enriched on the X chromosome. Sites that exhibit hypermethylation are enriched in promoters of genes involved in the regulation of metabolic processes. Unexpectedly, subordinate males have higher mortality rates than reproductively dominant males and exhibit faster DNAm change than dominants at dozens of sites. Our results reveal that differences in mortality associated with sex and social status are reflected by changes in DNA methylation, providing novel insights into mechanisms of aging and mortality in this and likely other wild animal populations.