The discovery of epigenetic mechanisms has ignited speculation into their role in ecological and evolutionary processes. In particular, the contribution of epigenetic variation to adaptation or phenotypic plasticity that is distinct from genetic variation would be an important addition to existing evolutionary mechanisms. Although the research of epigenetic mechanisms from an ecological and evolutionary (or eco-evolutionary) perspective has been growing, it is still unclear how epigenetic variation might function in natural populations and settings and to what extent it might serve to mediate population response to changing environmental conditions over time. Over the course of my dissertation, I explored the importance of DNA methylation in population response to a variety of environmental conditions. In the first chapter of my dissertation, I reviewed existing literature on the relationship between DNA methylation and environmental response. I argued that given the weight of current evidence, DNA methylation, in addition to other epigenetic mechanisms, needs to be included the evolutionary synthesis. Additionally, I identified a number of outstanding questions and outlined research directions that would help elucidate the role of epigenetic mechanisms in evolution. In my second chapter, I studied the genetic and epigenetic composition of populations of Spartina alterniflora that were impacted by the Deepwater Horizon oil spill in 2010. Current evolutionary theory predicts that following a severe environmental stressor, populations may experience a bottleneck effect, in which one or only a few genotypes survive to reproduce in subsequent generations. However, it is unclear whether these patterns are reflected in epigenetic variation as well, because novel environmental perturbations may serve to induce epigenetic variation rather than diminish it. We found a significant genetic signature of oil exposure in exposed populations, but did not see a similar effect in the epigenetic composition of exposed populations. These data suggest that epigenetic modifications, such as DNA methylation, may not always increase in number during stressful episodes, but may instead follow genetic variation. These results provide valuable information for the development of nascent population epigenetic theory, and may help parameterize expectations about conditions that provoke epigenetic variation, particularly when genetic variation may be limited. In addition to strong, unpredictable stressors, populations also respond via phenotypic changes over time through developmental stages and life histories that coincide with seasonal, regular environmental cues. Epigenetic mechanisms influence these regulatory and developmental changes that occur within an individual over time. In my third chapter, I examined the epigenetic response to seasonality in multiple coastal plant species. We found a weak signature of single methylation polymorphisms that was associated with seasonal environmental change within the studied species, as well as global patterns of methylation that were consistent across species. The results of this study indicate the possibility of conservation of methylation patterns across phylogenetic histories. In my fourth chapter, I explored in detail how the ability to maintain methylation might affect stress response. We compared individuals of the model plant Arabidopsis thaliana that were deficient in maintenance methylation machinery to control genotypes under both abiotic and biotic stresses, and then studied the growth of their offspring in the absence of stress. We found inherited phenotypic signatures of parental stress in the offspring generation and interactive effects of parental stress and genotype. This study not only reinforces the correlations that we observed in our field studies, but adds to the growing body of literature highlighting the importance of DNA methylation both in immediate environmental response and as a mechanism for heritability. Overall, this dissertation demonstrates that DNA methylation is highly abundant in natural populations and may be part of the response to various stressors at a number of time scales. The integration of DNA methylation in the evolutionary synthesis will aid in the explanation of phenomena such as phenotypic plasticity or adaptation, and will be an important contribution to the existing body of evolutionary mechanisms.