Female genitalia are widely underrepresented in taxonomic studies. Here we investigate the morphological variation among female copulation organs for a group of scarab beetles (Sericini) with similar ecology, external morphology and copulation mechanics. We examined traits qualitatively and quantitatively based on 80 and 18 species (genus Pleophylla), respectively. Additionally we explored whether female genitalia are affected by asymmetry. The vast diversity of slerotised structures including their shapes illustrated the high taxonomic and phylogenetic utility of female genitalia in this group. The morphometric analysis of Pleophylla, confirmed that sclerotisations in the ductus bursae are very suitable for species-level taxonomic purposes. Stable interspecific variation is more hardly discernable in other parts such as the vaginal palps (shape and size) or the other membranous structures such as the shape of the bursa copulatrix. Asymmetric genitalia that arose multiple times independently among insects are found in most of the examined Sericini species. Asymmetries regarded either the bursa copulatrix, or both the bursa copulatrix and ductus bursae and comprised sclerotised and non-sclerotised structures being most common in modern Sericini. Here, highly asymmetric sclerotised structures are linked with strong asymmetry of the male copulation organs. Widespread asymmetry among megadiverse Sericini with a complex male-female genital asymmetry suggests that the shift to asymmetry is phylogenetically rather conserved. From the range of hypotheses, sexual selection seems to be the most reasonable to explain the evolution and stability of asymmetry in chafer genitalia.