Epigenetic variation might play an important role in generating adaptive phenotypes by underpinning within-generation developmental plasticity, persistent maternal effects of the environment (e.g., trans-generational plasticity), or heritable epigenetically based polymorphism. These adaptive mechanisms should be most critical in organisms where sources of variation are limited. Consequently, using a clonally reproducing freshwater snail (Potamopyrgus antipodarum), we examined the plasticity of an adaptive phenotype (shell shape) and of DNA methylation between generations by experimentally manipulating the current-speed environment in the lab. By comparing three generations of lab-reared snails with reference field populations, we showed that habitat-specific adaptive shell shape is stable across one generation, and adaptively responds gradually over two subsequent generations. We also showed that DNA methylation specific to high-current environments was stable across one generation. Together these observations suggest that shell shape variation is at least in part determined by transgenerational plasticity and that DNA methylation provides a potential mechanism. Overall design: River snails were collected from tributary spring stream of the Snake River at Ritter Island (42.7439°N, 114.8420°W). For the transgenerational observations of shell shape, 5 iso-female lines were initiated. After the first generation reproduced, snails were photographed under a dissecting microscope and their tissue was harvested for analysis of DNA methylation. The second and third generations were raised under the same conditions and shell shapes were measured after females were reproductive.