Author summary The high mutation rate of RNA viruses makes it problematic to understand and resolve the role of recombination in generating genomic variation. Frequent mutations will (1) increase the likelihood of convergent mutations, particularly in regions subject to strong positive selection, causing sequence similarities that can be mistaken for recombination events, and (2) introduce new changes that accumulate and obscure recognition of past recombination events. We analyzed the patterns of recombination across Betacoronaviruses using a dedicated approach to distinguish true recombination from convergent mutations. The Betacoronaviruses comprise several populations that could be considered distinct biological species in that they do not engage in gene flow with one another. Moreover, recombination events within the Sarbecovirus subgenus, which includes SARS-CoV-2, are highly biased and predominate in the spike protein region, implicating recombination as having a substantial role in host tropism and viral ecology.