Wild bird–origin influenza A viruses (IAVs or avian influenza) have led to sporadic outbreaks among domestic poultry in the United States (US) and Canada, resulting in economic losses through the implementation of costly containment practices and destruction of birds. We used evolutionary analyses of virus sequence data to determine that 78 H5 low pathogenic avian influenza viruses (LPAIVs) isolated from domestic poultry in the US and Canada during 2001–2017 resulted from 18 independent virus introductions from wild birds. Within the wild bird reservoir, the hemagglutinin gene segments of H5 LPAIVs exist primarily as two co-circulating genetic sublineages, and our findings suggest the H5 gene segments flow within each migratory bird flyway and among adjacent flyways, with limited exchange between the non-adjacent Atlantic and Pacific Flyways. Phylogeographic analyses provided evidence that IAVs from dabbling ducks and swans/geese contributed to emergence of viruses among domestic poultry. H5 LPAIVs isolated from commercial farm poultry (i.e. turkey) were descended from a single introduction typically remain a single genotype, whereas those from live bird markets sometimes led to multiple genotypes, reflecting the potential for reassortment with other IAVs circulating within live bird markets. H5 LPAIV introduced from wild birds to domestic poultry represent economic threats to the U.S. poultry industry, and our data suggest that such introductions have been sporadic, controlled effectively through production monitoring and a stamping-out policy, and are, therefore, unlikely to result in sustained detections in commercial poultry operations.