Defining bacterial species and understanding the relative cohesiveness of different components of their genomes remains a fundamental problem in microbiology. Bacterial species tend to be comprised of both a set of core and dispensable genes, with the sum of these two components forming the species pan-genome. The role of the core and dispensable genes in defining bacterial species and the question of whether pan-genomes are finite or infinite remain unclear. Here we demonstrate, through the analysis of 96 genome sequences derived from two closely related sympatric sister species of pathogenic bacteria (Campylobacter coli and C. jejuni), that their pan-genome is indeed finite and that there are unique and cohesive features to each of their genomes defining their genomic identity. The two species have a similar pan-genome size; however, C. coli has acquired a larger core genome and each species has evolved a number of species-specific core genes, possibly reflecting different adaptive strategies. Genome-wide assessment of the level of lateral gene transfer within and between the two sister species, as well as within the core and non-core genes, demonstrates a resistance to interspecies recombination in the core genome of the two species and therefore provides persuasive support for the core genome hypothesis for bacterial species.