Streptococcus dysgalactiae subsp. equisimilis (SDSE) is increasingly recognised as a cause of human disease with the incidence of invasive disease and clinical manifestations comparable to the closely related Streptococcus pyogenes. Lateral gene flow of virulence markers has been previously documented, yet no systematic analyses has been undertaken to estimate the extent of gene overlap between these two human pathogens. To achieve this aim, we compiled a global database of 501 SDSE genomes and undertook comparative pangenomics with 2083 S. pyogenes genomes. We estimate 75% of core genes are common to these two pathogens of which one-third exhibited evidence of likely inter-species recombination. Sixteen of 55 mobile genetic element insertion regions in SDSE and 25% of clusters of elements at these regions were found in both SDSE and S. pyogenes. To investigate the potential impact of S. pyogenes vaccine candidates on SDSE, 12 of 34 preclinical vaccine antigens were found in >99% of isolates in both species including six with evidence of inter-species recombination. These findings demonstrate previously unappreciated levels of genomic overlap between these closely related organisms which has implications for streptococcal disease surveillance, pathobiology, and vaccines impact.