Epigenetic processes (e.g., DNA methylation) have been proposed as potentially important evolutionary mechanisms. However, before drawing conclusions about their evolutionary relevance, we need to evaluate the independence of epigenetic variation from genetic variation, as well as the extent of methylation polymorphism in nature. We evaluated these in natural populations of a clonal fish, Chrosomus eos-neogaeus, for which genetically identical individuals may be found in distinct environments. A genomic survey confirms the genetic uniformity of individuals, whereas a substantial level of inter-individual variation results in DNA methylation. Survey of the methylation status of the CpG dinucleotides of a fragment of a retrotransposon confirmed a marked difference in epiallelic composition among tissues, as well as among individuals. This study provides further evidence of epigenetic variation in the absence of genetic variation and demonstrates that this process can be a source of random variation in natural populations.