Campylobacter fetus subsp. fetus and C. fetus subsp. venerealis both cause disease in livestock but each subspecies generally occupy different specific host niches. C. fetus subsp. fetus is normally found in the gut while C. fetus subsp. venerealis in the genital tract of ruminants. C. fetus subsp. venerealis infections can cause abortion and infertility in cattle, while subsp. fetus is unlikely to result is such severe outcomes. To understand the molecular basis for such differences we sequenced the genomes of two C. fetus subsp. venerealis biovars (Venerealis and Intermedius) using Illumina technology. Our current draft assemblies suggest a similar genome size for both biovar genomes (~1.94Mbp) that are longer than the 1.77 Mbp genome of the reference C. fetus subsp. fetus ATCC 19438 genome. As compared to the C. fetus subsp. fetus genome 99kb and 94kb unique regions were found in the C. fetus subsp. venerealis Biovar Venerealis and Intermedius genomes, respectively. These sequences have been utilized to design biovar specific assays for diagnosis of field samples. The presence of a pathogenicity island (PAI) is known to be associated with the virulence of these strains, we identified unique features in the C. fetus subsp. venerealis bv. Venerealis PAI and a significant sequence divergence in the bv. Intermedius PAI. In the genome, we found a mutation in the alanine/glycine amino acid carrier protein (AACP) that correlates with the increased intolerance of C. fetus subsp. venerealis bv. Venerealis strains when grown in 1% glycine. This toxicity can be rescued with exogenous addition of Mg2+ ions or growth at pH 9.5. Finally, we found divergent flagellin genes in C. fetus subsp. venerealis bv. Venerealis that may increase robustness of the flagella and hence increase their motility fitness necessary to find a proper niche for their growth and/or enable colonization of placenta in cattle that results in abortion.