Abstract The ant genus Tapinoma Foerster, 1850 is a moderately diverse group (81 valid species) that occurs worldwide. It includes the tramp species T. melanocephalum, whose evolutionary history, biogeographic origin, and population limits remain unclear. Here, we present a time-calibrated phylogeny and a biogeographic history inference of the genus based on thousands of Ultraconserved Element (UCE) loci. Focusing on T. melanocephalum, we used single nucleotide polymorphisms from UCE loci and COI sequences to analyze species boundaries based on nuclear and mitochondrial DNA. We recovered a monophyletic Tapinoma with an estimated crown age corresponding to middle Eocene (49.4 to 34.4 Ma). Phylogenomic data differentiated T. melanocephalum from T. jandai, a recently established species based on morphology, and revealed that the 2 species diverged ∼12 Ma. Population genetic analyses identified considerable molecular divergence among sampled T. melanocephalum populations, and a heterogeneous genetic structure, showing a weak relationship between genetic differentiation and geographic distance. A phylogeographic comparison of habitat preferences of T. melanocephalum revealed an ecological shift from undisturbed to urban environments, a phenomenon which may have facilitated its ubiquitous and global distribution. Our study presents the first phylogenomic framework for this globally distributed ant genus and molecularly delineates a worldwide pest ant species.