In North America, Lyme disease (LD) is a tick-borne zoonosis caused by the spirochaete bacterium Borrelia burgdorferi sensu stricto (s.s.), which is maintained by wildlife. Tick vectors and bacteria are currently spreading into Canada and causing increasing numbers of cases of LD in humans and raising a pressing need for public health responses. There is no vaccine and LD prevention depends on knowing who is at risk and informing them how to protect themselves from infection. Recently, it was found in the USA that some strains of B. burgdorferi s.s. cause severe disease, whereas others cause mild, self-limiting disease. While many strains occurring in the USA also occur in Canada, strains in some parts of Canada are different than those in the USA. We therefore a a need to identify which strains specific to Canada can cause severe disease, and to characterize their geographic distribution to determine which Canadians are particularly at risk. In this review, we summarise the history of emergence of LD in North America, our current knowledge of B. burgdorferi s.s. diversity, its intriguing origins in the ecology and evolution of the bacterium, and its importance for the epidemiology, and clinical and laboratory diagnosis of LD. We propose methods for investigating associations between B. burgdorferi s.s. diversity, ecology and pathogenicity, and developing predictive tools to guide public health interventions. We also highlight the emergence of B. burgdorferi s.s. in Canada as a unique opportunity for exploring the evolutionary aspects of tick-borne pathogen emergence.