In the honey bee, Apis mellifera, DNA methylation is involved in various aspects of behaviour and development, such as regulating differentiation of the queen and worker castes1 . However, it may also be involved in other biological functions and contribute to parent-of-origin effects via genomic imprinting2 . To begin to tackle this question, we analysed the whole genome methylation profiles of honey bee unfertilised eggs, the adult drones that developed from these eggs, and the sperm the drones produced. These methylomes reveal distinct patterns of methylation. Eggs and sperm show 381 genes with significantly different CpG methylation patterns, with the vast majority being more methylated in egg. Drones show reduced levels of methylation across the genome when compared to both gamete samples, suggesting a cycle of methylation loss and gain throughout the development of the adult drone and during gametogenesis. The different methylation profiles in egg and sperm cells demonstrate that parent-specific marking of honey bee gametes occurs. We discuss the potential developmental and evolutionary outcomes of differential methylation and how this may relate to predictions of the kinship theory of genomic imprinting in this eusocial insect.