Understanding speciation is a fundamental goal in evolutionary biology. Genomic regions of accentuated differentiation among populations often reveal patterns and mechanisms of species formation. While substantial progress has been achieved on this front for genetic variation, the contribution of epigenetic mechanisms to divergence patterns remains unclear. Here, we present evidence that DNA methylation is associated with regions exhibiting accentuated genetic differentiation between populations of Timema cristinae stick insects. We do so by integrating analyses of differentially methylated regions (DMRs) between individuals from different host-plant species with genomic sequencing. Our results reveal that DMRs exhibit accentuated genetic differentiation (FST) between populations. Strikingly, the strength of this association increases with the geographical distance between populations. We present results evaluating the contributions of mutation, reduced recombination, gene flow and selection to these divergence patterns. The overall results are consistent with a role for a balance between selection and gene flow, a finding further supported by evidence for selection in a previously-published survival field experiment. Nevertheless, details of our results suggest that selection on DMRs might be indirect and not strictly host-related. Our results establish associations between methylation and genetic change, but further work is required to clarify the exact causes of this association. Nonetheless, our results provide insight into how the interplay of epigenetic and genetic variation may influence population divergence and potentially contribute to speciation.