We examined adaptive morphological divergence and epigenetic variation in genetically impoverished asexual populations of a freshwater snail, Potamopyrgus antipodarum from distinct environments. These populations exhibit environment-specific adaptive divergence in shell shape and significant genome wide DNA methylation differences among differentially adapted lake and fast water flow river populations. The epigenetic variation correlated with adaptive phenotypic variation in rapidly adapting asexual animal populations. This provides one of the first examples of environmentally-driven differences in epigenetics that associates with adaptive phenotypic divergence. Overall design: To examine the association between this adaptive divergence and epigenetic differences, we sampled at least 30 individuals from a “river” site characterized by constantly fast water current speeds due to input from underground springs (Ritter Island, Snake River, ID) and from a “lake” site with no water current (Lake Lytle, Rockaway Beach, OR). Shell spire height and aperture length were measured as an index of adaptive foot size and shell shape differences. On these same samples, we dissected foot tissue from individuals for the analysis of epigenetic variation.