The flat wasp Apenesia Westwood is one of the largest genera in Pristocerinae with 190 species worldwide. The lack of a single diagnostic morphological character has resulted in many distinct ground plans within Apenesia. Some authors have suggested Apenesia as polyphyletic. Here we aimed to investigate and delimit the genus based on morphological and molecular data. We analysed 163 morphological characters on tnt using ‘traditional search’, whereas Bayesian (BI) and maximum likelihood (ML) inferences were performed on 1553 concatenated nucleotide base pairs from COI and 28S sequences. Apenesia was recovered as polyphyletic in all analyses with up to 10 different lineages spread throughout the tree. We mapped female morphological characters onto the molecular tree to enlighten morphological evolution in the apterous females. Based on our morphological and molecular analyses, and on the taxonomic revision of holotypes and specimens, we propose six new genera in the Pristocerinae and revalidate the generic status of two: Acrenesia gen.n., Austranesia gen.n., Cleistepyris stat. rev., Dracunesia gen.n., Eleganesia gen.n., Epynesia gen.n., Pristonesia gen.n., and Propristocera stat. rev. We also propose four new generic synonymies: Neoapenesia syn.n. under Apenesia, Dipristocera syn.n. under Cleistepyris, Afrocera syn.n. and Neopristocera syn.n. under Propristocera. At the species level, we indicate Apenesia minor syn.n. under Propristocera tagala. In all, 162 new combinations, eight reinstated combinations and one new name to avoid homonymy are proposed. Apenesia is now defined as flat wasps having males with the mesoscutum gibbous, the genitalia with the paramere narrow and densely hairy, and the aedeagus with the ventral apical lobe elliptical and covered with lumps. Females of Apenesia can be distinguished from other Pristocerinae by having the head wider than the mesosoma, the antennae short, the mandible long, and the clypeus surpassing the toruli in the frons. This study reinforces the difficulties in defining Apenesia and other Pristocerinae genera. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:65FB3087‐0F30‐4851‐B1BA‐ED6E4518B958. We reconstructed molecular and morphological phylogenies of Pristocerinae (Bethylidae) flat wasps with the emphasis on the genus Apenesia, proposing six new genera in Pristocerinae, revalidating two and synonymizing four. We discuss the extreme sexual dimorphism in the subfamily, mapping the female's characters onto the molecular tree. Our results reveal novel morphological characteristics to distinguish genera within Pristocerinae and reinforce the difficulties in defining Apenesia and the importance of an integrative taxonomy.