The formation of stomata is known to be influenced by environmental conditions including light, CO2 and humidity, and the environmental signal has been shown to elicit both systemic and heritable responses. Plants, nevertheless, maintain plasticity in their capacity to moderate stomatal density during subsequent leaf growth. We hypothesized that the plastic element of stomatal formation could be under epigenetic control. In this way, gene expression patterns could be faithfully copied cell-to-cell and inherited in a non-Mendelian fashion. Plant flowering response to extremes of temperature is known to be epigenetically controlled in Arabidopsis and cytosine DNA methylation is an important mechanism epigenetically silencing genomic elements and regulating gene expression. We induced a reduced stomatal index in Arabidopsis by controlling percentage relative humidity (RH) and investigated methylation of known genes in stomatal formation and patterning pathways, using methylation-specific qPCR and high resolution melt analysis following bisulphite treatment. Two target genes involved in stomatal formation pathways were differentially methylated between treatments. Furthermore, stomatal density in the following, seminal generation of plants exposed to both RH percentages varied according to parental treatment. We present these data and explore the implications of epigenetic control of stomatal density.