West Nile virus (WNV) entered North America in 1999, with its subsequent spread across the continent in the next three years having a major impact on local bird populations. WNV represents therefore a classic example of a virus establishing itself in a new geographic and host environment. However, despite the impact of WNV in North America, the pattern and dynamics of its spatial spread remain uncertain, particularly whether the virus encountered major barriers as it spread from East-to-West across the continental USA, or was able to do so in an unconstrained manner. To address this key question in WNV molecular epidemiology we sequenced the complete genomes of approximately 300 avian isolates of WNV sampled across the USA over a period of 11 years (2001-2012). Phylogenetic analysis revealed that the initial NY99 genotype split into two sister clades that initially circulated in different regions. However, one clade (WN02), characterized by an amino acid substitution that favours transmission in mosquitoes, quickly spread across the USA, replacing every other genotype. This explosive spread of WNV is supported by the lack in evident clustering according to geographical distribution, or year of isolation, although there was clustering according to host species (mosquitoes versus birds). An apparent of absence of adaptive evolution during this emergence is also manifest with low rates of nonsynonymous to synonymous substitutions across the viral genome, suggesting that the majority of lineages are of equal fitness. In sum, the molecular epidemiology of WNV in North America depicts an unfettered expansion within a permissive host and geographic population with no evidence of major adaptive barriers.