Footrot is a contagious disease of the feet of sheep and other ruminants. The disease has long been recognised as a problem in sheep producing countries, causing major economic losses. The severity of disease ranges from an interdigital dermatitis (benign footrot), to underrunning of the horn of the hoof and separation of the horn from the underlying tissue (virulent footrot), which leads to lameness and loss of body condition. The principal causative agent of footrot is the bacterium Dichelobacter nodosus, an anaerobic, gram negative rod, and strains are classified as benign or virulent based on their ability to degrade elastin and their protease thermostability. We have sequenced the genomes of 103 D. nodosus isolates from eight different countries. Comparison of these genomes revealed that they are highly conserved, with > 95% sequence identity. Sequence variation was largely confined to eight major regions that have been identified as areas of atypical trinucleotide composition in the sequenced reference strain, VCS1703A. Analysis of conserved regions of these genomes based on read mapping to this reference sequence identified 31,627 sites that were present in all of the sequenced strains and varied in one or more of these strains. Using this single nucleotide polymorphism data set as the basis for the inference of phylogenic relationships we observed that D. nodosus strains separated into two distinct clades, irrespective of their geographic origin. This division generally correlated with the known virulent and benign phenotypes, as well as with the single amino acid difference between the AprV2 and AprB2 proteases, which are produced by virulent and benign strains, respectively. These inferred relationships provide evidence that virulent and benign strains of D. nodosus exist as two separate lineages worldwide. These observations will have impact on the future directions of the management and targeted control of virulent ovine footrot.