Epigenetic maternal effects are being studied in laboratories at an exponentially increasing rate and have routinely been found to have consequences on the physiological and behavioural function of mammalian offspring. Despite this wealth of knowledge, our understanding of how epigenetic maternal effects impact free-living animals within natural ecosystems is comparatively non-existent. Here, I examine laboratory epigenetic maternal effects literature from the last decade with a perspective informed by an eco-evolutionary framework and found that the type and timing of maternal effects influences the extent of offspring DNA methylation in mammals. Additionally, I use an innovative experimental field manipulation to assess the epigenetic maternal effects of stress in free-living North American red squirrels and found inherent sex-specific differences in Nr3c1 and Pomc gene expression of red squirrel offspring despite no effect of maternal stress. Together, these studies highlight the importance of integrating evolutionary, ecophysiological, and molecular theory when studying epigenetic maternal effects.