The extent, pattern and basis of epigenomic variation were explored in this study through characterization of genomes, methylomes and transcriptomes of wild populations of Arabidopsis thaliana. The findings suggest that single cytosine methylation polymorphisms do not have a genetic basis in this species. However, genetic variation does affect RNA-directed DNA methylation (RdDM) that occurs at differentially methylated regions, for which thousands of methylation quantitative trait loci were identified. Targets of RdDM, including protein-coding genes, were found to be activated in pollen and seeds, which may be important for developmental functions.