Significance Changes in the methylation status of cytosine nucleotides are a source of heritable epigenetic and phenotypic diversity in plants. Here we derive robust estimates of the rate at which cytosine methylation is spontaneously gained (forward epimutation) or lost (backward epimutation) in the genome of the model plant Arabidopsis thaliana . We show that the forward–backward dynamics of selectively neutral epimutations have a major impact on methylome evolution and shape genome-wide patterns of methylation diversity among natural populations in this species. The epimutation rates presented here can serve as reference values in future empirical and theoretical population epigenetic studies in plants. Stochastic changes in cytosine methylation are a source of heritable epigenetic and phenotypic diversity in plants. Using the model plant Arabidopsis thaliana , we derive robust estimates of the rate at which methylation is spontaneously gained (forward epimutation) or lost (backward epimutation) at individual cytosines and construct a comprehensive picture of the epimutation landscape in this species. We demonstrate that the dynamic interplay between forward and backward epimutations is modulated by genomic context and show that subtle contextual differences have profoundly shaped patterns of methylation diversity in A. thaliana natural populations over evolutionary timescales. Theoretical arguments indicate that the epimutation rates reported here are high enough to rapidly uncouple genetic from epigenetic variation, but low enough for new epialleles to sustain long-term selection responses. Our results provide new insights into methylome evolution and its population-level consequences.