Dogs are uniquely associated with human dispersal and bring novel insight into human migration and the domestication process. Dingoes represent an intriguing case within canine evolution being geographically isolated for thousands of years. Here we present a high-quality de novo assembly of a pure dingo which gives a multi-thousand-year-old snapshot in the evolutionary history of dogs. Using multiple long read sequencing technologies, we identified large chromosomal differences relative to the current dog reference (CanFam3.1) and confirmed no expanded pancreatic-amylase gene as found in all breed dogs. Phylogenetic analyses using variant pairwise matrices show that the dingo is distinct from breed dogs with 100% bootstrap support when using Greenland wolf as the outgroup. Functionally, we observe differences in methylation patterns between the dingo and German Shepherd Dog genomes and differences in serum biochemistry and microbiome makeup. Our results suggest that distinct demographic and environmental conditions have shaped the dingo genome. In contrast, artificial human selection has likely shaped the genomes of domestic breed dogs after divergence from the dingo. This work shows, for the first time, that the dingo is truly an early offshoot of modern dogs situated between the grey wolf and the domesticated dogs of today. These findings have implications for conservation of this unique Australian animal. The new dingo genome additionally represents a potential model for breed-specific diseases with such diseases arising due to artificial selection in the last 200 years since the divergence of dingoes.