The H3N2 canine influenza virus (CIV) emerged from an avian reservoir in Asia to circulate entirely among dogs for the last 20 years. The virus was first seen circulating outside Asian dog populations in 2015, in North America. Utilizing viral genomic data in addition to clinical reports and diagnostic testing data, we provide an updated analysis of the evolution and epidemiology of the virus in its canine host. CIV in dogs in North America is marked by a complex life history - including local outbreaks, regional lineage die-outs, and repeated reintroductions of the virus (with diverse genotypes) from different regions of Asia. Phylogenetic and Bayesian analysis reveal multiple CIV clades, and viruses from China have seeded recent North American outbreaks, with 2 or 3 introductions in the past 3 years. Genomic epidemiology confirms that within North America the virus spreads very rapidly among dogs in kennels and shelters in different regions - but then dies out locally. The overall epidemic therefore requires longer-distance dispersal of virus to maintain outbreaks over the long term. With a constant evolutionary rate over 20 years, CIV still appears best adapted to transmission in dense populations and has not gained properties for prolonged circulation among dogs.