Ovine footrot is a contagious disease of the feet of sheep. The disease has long been recognised as a problem in sheep producing countries, causing major economic losses. 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) leading 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 using next generation sequencing technology. Comparison of these genomes revealed that they are highly conserved, with > 95% sequence identity. Sequence variation was largely confined to eight major regions that had previously 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 32,448 sites that were present in all of the sequenced strains and varied in one or more of these strains. Using this data set as the basis for the inference of phylogenic relationships we observed that strains separated into two distinct clades, irrespective of geographic origin. This division correlated with the known benign and virulent 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 suggest that benign and virulent strains of D. nodosus exist as two separate lineages worldwide. These observations will have substantial impact on future directions of the management and targeted control of virulent ovine footrot.