Recent genome-wide DNA methylation analyses of insect genomes accentuate an intriguing contrast compared with those in mammals. In mammals, most CpGs are heavily methylated, with the exceptions of clusters of hypomethylated sites referred to as CpG islands. In contrast, DNA methylation in insects is localized to a small number of CpG sites. Here, we refer to clusters of methylated CpGs as "methylation islands (MIs)," and investigate their characteristics in seven hymenopteran insects with high-quality bisulfite sequencing data. Methylation islands were primarily located within gene bodies. They were significantly overrepresented in exon-intron boundaries, indicating their potential roles in splicing. Methylated CpGs within MIs exhibited stronger evolutionary conservation compared with those outside of MIs. Additionally, genes harboring MIs exhibited higher and more stable levels of gene expression compared with those that do not harbor MIs. The effects of MIs on evolutionary conservation and gene expression are independent and stronger than the effect of DNA methylation alone. These results indicate that MIs may be useful to gain additional insights into understanding the role of DNA methylation in gene expression and evolutionary conservation in invertebrate genomes.