Staphylococcus pseudintermedius is a commensal bacterium and a major opportunistic pathogen of dogs. The emergence of methicillin-resistant S. pseudintermedius (MRSP) is also becoming a serious concern. We carried out a population genomics study of 130 clinical S. pseudintermedius isolates from dogs and cats in the New England region of the United States. Results revealed the co-circulation of phylogenetically diverse lineages that have access to a large pool of accessory genes. Many MRSP and multidrug-resistant clones have emerged through multiple independent, horizontal acquisition of resistance determinants and frequent genetic exchange that disseminate DNA to the broader population. When compared to a Texas population, we found evidence of clonal expansion of MRSP lineages that have disseminated over large distances. These findings provide unprecedented insight into the diversification of a common cutaneous colonizer of man's oldest companion animal and the widespread circulation of multiple high-risk resistant clones.