is a major human opportunistic bacterial pathogen and a close relative of the recently established species . As a species, commensal remains relatively understudied, and its genetic connectivity with is not thoroughly understood. Here, we introduce a large collection of whole-genome sequenced isolates comprising 894 and 392 genomes. Using these genomes to complement publicly available data, we studied the genome content and the evolutionary relationship between these species. A wider range of host species was observed in ; in particular, there is a radiation of clades specialized to domesticated and pet animals among which is uncommon. Of note, pangenome analyses reveal that has significantly more allelic variation and lower recombination rates in core genes compared with . These observations suggest that represents a population that has occupied its ecological niche longer than has. This study enhances understanding of the evolutionary histories of these species and highlights the importance of sampling and studying closely related commensal bacteria in addition to clinically relevant opportunistic pathogens.