The continued evolution of bacterial pathogens has major implications for both human and animal disease, but the
exchange of genetic material between host-restricted pathogens is rarely considered. Streptococcus equi subspecies equi (S.
equi) is a host-restricted pathogen of horses that has evolved from the zoonotic pathogen Streptococcus equi subspecies
zooepidemicus (S. zooepidemicus). These pathogens share approximately 80% genome sequence identity with the important
human pathogen Streptococcus pyogenes. We sequenced and compared the genomes of S. equi 4047 and S. zooepidemicus
H70 and screened S. equi and S. zooepidemicus strains from around the world to uncover evidence of the genetic events that
have shaped the evolution of the S. equi genome and led to its emergence as a host-restricted pathogen. Our analysis
provides evidence of functional loss due to mutation and deletion, coupled with pathogenic specialization through the
acquisition of bacteriophage encoding a phospholipase A2 toxin, and four superantigens, and an integrative conjugative
element carrying a novel iron acquisition system with similarity to the high pathogenicity island of Yersinia pestis. We also
highlight that S. equi, S. zooepidemicus, and S. pyogenes share a common phage pool that enhances cross-species pathogen
evolution. We conclude that the complex interplay of functional loss, pathogenic specialization, and genetic exchange
between S. equi, S. zooepidemicus, and S. pyogenes continues to influence the evolution of these important streptococci.