G. anatis bv. hemolytica (GAH) is an opportunistic pathogen causing peritonitis and salpingitis in chickens worldwide. It’s close relative G. anatis bv. anatis and the remaining Gallibacterium species are less common or are non-pathogenic to chicken. The population structure and recombination rates of Gallibacterium within and between the species level remains poorly characterized. In this study, broad-scale genomic comparison of 33 diverse Gallibacterium strains was conducted in order to identify evolutionary events leading to host specificity and pathogenicity of Gallibacterium. Based on sequence similarity and core SNPs phylogeny all Gallibacterium species were separated into two major groups. First group included three species sharing 51% to 79% core genome sequence homology, and second - two species sharing only 21-25% of the core genome with GAH. The latter group did not carry the major virulence factors known to be important in the pathogenesis in chickens (e.g. GtxA, Flf1A-Flf4A), but encoded several novel types of fimbria. Within GAH, phylogenetically all chicken strains were grouped separately from geese and ducks strains. In addition, chicken strains formed clusters based on the country of isolation. Pair-wise genome comparison enabled identification of up to 11 biovar, host or country specific genes, predominantly of the unknown function. Further analysis revealed that recombination is uncommon between distantly related strains, however it exceeds mutations between closely related strains of Gallibacterium. A number of lineage specific recombination hotspots likely occurred before delineation were detected. We identified from up to 11 regions affected by recombination between the strains isolated from different hosts of those previously shown to be highly pathogenic. These hotspots included mobile elements, adhesins, proteins involved in stress response or GTX toxin export. In conclusion, our findings indicate that host switch could play a role in Gallibacterium speciation, and recombination likely contributed to the divergence of Gallibacterium.