The role of the epigenome in phenotypic plasticity is unclear presently. Here we used a multiomics approach (RNA-seq, ChIP-seq, ATAC-seq and Hi-C) to explore the nature of the epigenome in developing honeybee (Apis mellifera) workers and queens. Our data showed that the distinct queen and worker epigenomic landscapes form during the developmental process. Differences in gene expression between workers and queens precede other epigenomic modifications, but the epigenomic differences between workers and queens become more extensive and more layered during development. Genes known to be important for caste differentiation were more likely to be multiply differentially regulated by more than one epigenomic system than other differentially expressed genes. This indicates a multidimensional regulation of expression of key genes, presumably to canalise differences in gene expression. Our data indicate that the epigenome interacts with diverging developmental trajectories rather than controlling them since different epigenomic landscapes form in concert with different developmental outcomes.