Thigmomorphogenesis is a plant acclimation response to short repetitive bursts of mechanical or touch stimulation. Touching plant organs elicits a transient ion signalling cascade that leads to rapid changes in gene expression. The underlying molecular mechanisms that coordinate the long-term morphological changes to repetitive mechanical stimulation are enigmatic. We recently reported how a chromatin-modifying enzyme, SDG8/ASHH2 can regulate the permissive expression of many mechanical responsive genes in Arabidopsis. The loss-of-function sdg8 mutant reduced the maximum levels of touch inducible gene expression. sdg8 mutants showed a perturbation in morphological response to wind-agitated mechanical stimulation, which implicated epigenetic memory forming processes in the acclimation response of thigmomorphogenesis (Cazzonelli et al., Frontiers in Plant Science, 2014). Here we analysed the effect of SDG8 on the genome-wide DNA methylation patterns in the presence and absence of FRIGIDA, which interacts with SDG8 to promote a vegetative to reproductive morphological transition in some Arabidopsis accessions. The sdg8 mutation reduced CG and enhanced CHG as well as CHH context dependent methylation. Introgression of FRIGIDA into the wild type columbia ecotype had no affect upon genome-wide DNA methylation, however restored CHG and CHH methylation back to wild type levels in the sdg8 mutant. We identified significant differential DNA methylation in genes involved in mechanical signalling and jasmonic acid processes. We describe how cross-talk between permissive chromatin modification and DNA methylation may be required to facilitate epigenetic memory-forming processes controlling morphological acclimation to prolonged environmental stimulation.