Background: Bovine tuberculosis (bTB) is a costly epidemiologically complex, multi-host, endemic disease. Lack of understanding of transmission dynamics may undermine eradication efforts. Pathogen whole genome sequencing improves epidemiological inferences, providing a means to determine the relative importance of inter- and intra- species host transmission for disease persistence. We sequenced an exceptional data set of 619 Mycobacterium bovis isolates from badgers and cattle in a 100km2 bTB hotspot in Northern Ireland. Historical molecular subtyping data permitted the targeting of an endemic pathogen lineage, whose long-term persistence provided a unique opportunity to study disease transmission dynamics in unparalleled detail. Additionally, to assess whether badger population genetic structure was associated with the spatial distribution of pathogen genetic diversity, we microsatellite genotyped hair samples from 769 badgers trapped in this area. Results: Graph transmission tree methods and structured coalescent analyses indicated the majority of bacterial diversity was found in the local cattle population. Results pointed to transmission from cattle to badger being more common than badger to cattle. Furthermore, the presence of significant badger population genetic structure in the landscape was not associated with the spatial distribution of M. bovis genetic diversity, suggesting that badger-to-badger transmission may not be a key determinant of disease persistence. Significance: Our data were consistent with badgers playing a smaller role in the maintenance of M. bovis infection in this study site, compared to cattle. Comparison to other areas suggests that M. bovis transmission dynamics are likely to be context dependent, and the role of wildlife difficult to generalise.