Epigenetic gene control is maintained by chromatin-associated Polycomb group (PcG) and Trithorax group (TrxG) genes, which act antagonistically via the interplay between PcG and TrxG regulation to generate silenced or permissive transcriptional states. In this study, we searched for PcG/TrxG genes in 180 arthropod genomes, covering all the sequenced arthropod genomes at the time of conducting this study, to perform a global investigation of PcG/TrxG genes in a phylogenetic frame. Results of ancestral state reconstruction analysis revealed that the ancestor of arthropod species has an almost complete repertoire of PcG/TrxG genes, and most of these genes were seldom lost above order level. The domain diversity analysis indicated that the PcG/TrxG genes show variable extent of domain structure changes; some of these changes could be associated with lineage-specific events. The likelihood ratio tests for selection pressure detected a number of PcG/TrxG genes which underwent episodic positive selection on the branch leading to the insects with holometabolous development. These results suggest that, despite their high conservation across arthropod species, different members of PcG/TrxG genes showed considerable differences in domain structure and sequence divergence in arthropod evolution. Our cross species comparisons using large-scale genomic data provide insights into divergent evolutionary pattern on highly conserved genes in arthropods.