Mounting evidence supports the view that the responses of plants to environmental stress are mediated by epigenetic factors, including DNA methylation. Understanding the relationships between DNA methylation, plant development and individual fitness under contrasting environments is key to uncover the potential impact of epigenetic regulation on plant adaptation. Experimental approaches that combine a controlled alteration of epigenetic features with exposure to some relevant stress factor can contribute to this end. We combined the experimental application of a demethylating agent (5-azacytidine) with recurrent drought, and recorded their effects on above- and below-ground phenotypic traits related to early development, phenology and fitness inErodium cicutariumfrom two provenances. We found that 5-azacytidine significantly reduced DNA methylation in leaf and root tissues. Moreover, it slowed plant development, delayed flowering, and reduced the number of inflorescences produced, and such detrimental effects occurred independently of water regime. Recurrent drought reduced final above- and below-ground biomass and total inflorescence production, and such negative effects were unaffected by artificial changes in DNA methylation. Increased fruit and seed-set were the only adaptive responses to drought observed inE. cicutarium, together with an increased number of flowers per inflorescence recorded in water stressed plants previously treated with 5-azacytidine. Thus, epigenetic effects can desynchronize plant growth, flowering and senescence among individual plants in both favourable and adverse environments. Future studies should focus on understanding intraspecific variation in the ability to change plant methylome in response to stress.