is a common cause of food-borne gastroenteritis worldwide. Recent work defining the phylogeny of the genus subdivided into six distinct phylogroups. Here, we provide detailed analyses of the evolutionary processes leading to the emergence of these phylogroups. The dominant phylogroups isolated from human infections, PG3-5, show very little diversity at the sequence level, but do present marked patterns of gain and loss of functions, including those involved in pathogenicity and metabolism, including the acquisition of phylogroup-specific O-antigen loci. We tracked gene flow across the species in the core and accessory genome, and show that the non-pathogenic PG1 strains act as a reservoir for diversity, frequently acting as donors in recombination events. Analysis of the core and accessory genome also suggested that the different phylogroups may be ecologically separated, in contrast to the long-held belief of common shared ecological niches across the species.