Abstract Detailed osteological descriptions of the craniomandibular complex of passerine birds are lacking for most species, limiting our understanding of their diversity and evolution. Cowbirds (genus Molothrus ) are a small but widespread group of New World nine‐primaried songbirds, well‐known for their unique brooding parasitic behavior. However, detailed osteological data for cowbirds and other Icteridae are currently scarce and several features of their skulls remain undescribed or poorly known. To address this issue, a detailed comparative osteology of cowbird skulls is presented here for the first time based on data from x‐ray microcomputed tomography, dry skeletal data, and multivariate analyses of linear morphometric data. Cowbird skulls offer some functional insights, with many finch‐like features probably related to a seed‐rich diet that distinguishes them from most other icterids. In addition, features previously overlooked in earlier studies might provide valuable phylogenetic information at different levels of passerine phylogeny (Passerida, Emberizoidea, Icteridae, and Agelaiinae), including some of the otic region and nasal septum. Comparisons among cowbirds show that there is substantial cranial variation within the genus, with M. oryzivorus being the most divergent cowbird species. Within the genus, distantly related species share similar overall skull morphology and proportions, but detailed osteological data allow species identification even in cases of strong convergence. Further efforts are warranted to furnish baseline data for future studies of this iconic group of Neotropical birds and to fully integrate it into phylogenetic comparative frameworks.