Variation in DNA methylation patterns among genes, individuals, and populations appears to be highly variable among taxa, but our understanding of the functional significance of this variation is still incomplete. We here present the first whole genome bisulfite sequencing of a chelicerate species, the social spider Stegodyphus dumicola. We show that DNA methylation occurs mainly in CpG context and is concentrated in genes. This is a pattern also documented in other invertebrates. We present RNA sequence data to investigate the role of DNA methylation in gene regulation and show that, within individuals, methylated genes are more expressed than genes that are not methylated and that methylated genes are more stably expressed across individuals than unmethylated genes. Although no causal association is shown, this lends support for the implication of DNA CpG methylation in regulating gene expression in invertebrates. Differential DNA methylation between populations showed a small but significant correlation with differential gene expression. This is consistent with a possible role of DNA methylation in local adaptation. Based on indirect inference of the presence and pattern of DNA methylation in chelicerate species whose genomes have been sequenced, we performed a comparative phylogenetic analysis. We found strong evidence for exon DNA methylation in the horseshoe crab Limulus polyphemus and in all spider and scorpion species, while most Parasitiformes and Acariformes species seem to have lost DNA methylation.