Parental effects influence offspring phenotypes through pre- and post-natal routes but little is known about their molecular basis, and therefore their adaptive significance. Epigenetic modifications, which control gene expression without changes in the DNA sequence and are influenced by the environment, may contribute to parental effects. Taking advantage of the self-fertilising and inbred nature of the mangrove killifish Kryptolebias marmoratus, we investigated the effects of the rearing environment on parents and offspring by comparing neophobia, metabolic rate and brain epigenetic (DNA methylation) patterns of genetically identical fish reared in enriched or barren environments. Parental fish reared in enriched environments had lower cortisol levels, lower metabolic rates and were more active and neophobic than those reared in barren environments. They also differed in 1,854 methylated cytosines (DMCs). Offspring activity and neophobia were determined by the parental environment and we also found evidence of, limited but significant, parental influence on the DNA methylation patterns of the offspring. Among the DMCs of the parents, 98 followed the same methylation patterns in the offspring, three of which were significantly influenced by parental environments irrespective of their own rearing environment. Our results suggest that the environment experienced by the parents influences the behaviour and, to some extent, brain DNA methylation patterns of the offspring in an environment-specific manner.