Abstract The genus Chelonus Panzer is one of the largest genera within the subfamily Cheloninae with 11 subgenera and more than 1000 valid species. However, the phylogenetic relationships of species within this genus and their coevolutionary relationships with endogenous bracoviriforms (BVfs) remain unclear. Here we provide the first phylogenomic analysis of 42 taxa representing all 11 subgenera of Chelonus and other species within the Cheloninae using 2380 loci of ultraconserved elements (UCEs). The results showed that the subgenus Arichelonus Viereck has an isolated position outside of the rest of Chelonus , while the other 10 subgenera formed a monophyletic group, the traditional genus Chelonus . Four subgenera within Chelonus , that is, Chelonus s. str., Megachelonus Baker, Microchelonus Szépligeti and Parachelonus Tobias are polyphyletic, suggesting that the traditional genus Chelonus could be further divided into 14 clades. Divergence time estimates indicated that the subgenus Arichelonus diverged approximately 35.5 million years ago, while most species within the genus Chelonus diversified <21.9 million years ago. Ancestral state reconstructions revealed morphological innovations of the subfamily, including metasomal curvature, which may be linked to host‐use strategies. Cophylogenetic analyses demonstrated that a strong congruence of parasitoid‐bracoviriform exists and confirmed that BVf nudivirus genes and virulence genes displayed different evolutionary trajectories. Altogether, our findings provide new insights into the evolutionary history of the genus Chelonus and substantiated the coevolutionary relationships between the parasitoids and their associated BVfs.
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