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Variation of DNA methylation is thought to play an important role for rapid adjustments of plant populations to dynamic environmental conditions, thus compensating for the relatively slow response time of genetic adaptations. However, genetic and epigenetic variation of wild plant populations has not yet been directly compared in fast changing environments. Here, we surveyed populations of Viola elatior from two adjacent habitat types along a successional gradient characterized by strong differences in light availability. Using amplified fragment length polymorphisms (AFLP) and methylation-sensitive amplification polymorphisms (MSAP) analyses, we found relatively low levels of genetic (H'gen = 0.19) and epigenetic (H'epi = 0.23) diversity and high genetic (ϕST = 0.72) and epigenetic (ϕST = 0.51) population differentiation. Diversity and differentiation were significantly correlated, suggesting that epigenetic variation partly depends on the same driving forces as genetic variation. Correlation-based genome scans detected comparable levels of genetic (17.0%) and epigenetic (14.2%) outlier markers associated with site specific light availability. However, as revealed by separate differentiation-based genome scans for AFLP, only few genetic markers seemed to be actually under positive selection (0-4.5%). Moreover, principal coordinates analyses and Mantel tests showed that overall epigenetic variation was more closely related to habitat conditions, indicating that environmentally induced methylation changes may lead to convergence of populations experiencing similar habitat conditions and thus may play a major role for the transient and/or heritable adjustment to changing environments. Additionally, using a new MSAP-scoring approach, we found that mainly the unmethylated (ϕST = 0.60) and CG-methylated states (ϕST = 0.46) of epiloci contributed to population differentiation and putative habitat-related adaptation, whereas CHG-hemimethylated states (ϕST = 0.21) only played a marginal role.