Evolution by natural selection can occur when organisms harbor genetically inherited phenotypic variation, and phenotypic variants have differential fitness. Stable transgenerational epigenetic variation also exists for fitness-related traits and theory predicts that selection can act on this variation alone without a contribution of genetic variation. Here, we artificially selected for divergent rosette size and plant height in experimental Arabidopsis thaliana populations harboring DNA methylation polymorphism in an identical genetic background. We found significant epi-allele frequency changes in response to selection. Our results show how selection changed population trait values and their epigenetic basis in real time, over one generation of selection. Our results imply the role of the transgenerational epigenetic variation of populations as an additional source of short-term adaptive potential.