Populations of invasive species that colonize and spread in novel environments may differentiate both through demographic processes and local selection. European starlings (Sturnus vulgaris) were introduced to New York in 1890 and subsequently spread throughout North America, becoming one of the most widespread and numerous bird species on the continent. Genome-wide comparisons across starling individuals and populations can identify demographic and/or selective factors that facilitated this rapid and successful expansion. We investigated patterns of genomic diversity and differentiation using reduced-representation genome sequencing (ddRADseq) of 17 winter-season starling populations. Consistent with this species’ high dispersal rate and rapid expansion history, we found low geographic differentiation and few FST outliers even at a continental scale. Despite starting from a founding population of approximately 180 individuals, North American starlings show only a moderate genetic bottleneck, and models suggest a dramatic increase in effective population size since introduction. In genotype-environment associations we found that ~200 single-nucleotide polymorphisms are correlated with temperature and/or precipitation against a background of negligible genome- and range-wide divergence. Local adaptation in North American starlings may have evolved rapidly even in this wide-ranging and evolutionarily young population. This survey of genomic signatures of expansion in North American starlings is the most comprehensive to date and complements ongoing studies of world-wide local adaptation in these highly dispersive and invasive birds.