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Ixodes scapularis is responsible for the transmission of a variety of pathogens in North America, including Borrelia burgdorferi sensu stricto, Anaplasma phagocytophilum and Babesia microti. Songbirds have previously been described as agents of tick dispersal, and a combination of empirical data and modeling efforts have implicated songbirds in the range expansion of I. scapularis northward into Canada during spring bird migration. The role of fall bird migration has received comparatively less attention, particularly at a continental scale. The aim of the current research was to use a novel individual-based modeling approach (IBM) to investigate the role of southward migrating songbirds in the dispersal of I. scapularis within the continental United States. The IBM used in this research explicitly models dispersal by two extensively studied migrating songbird species, wood thrush Hylocichla mustelina and ovenbird Serums aurocapillus. Our IBM predicts the annual dispersal of more than four million ticks by H. mustelina and S. aurocapillus, notably into areas as far west as the Dakotas, and as far south as Central Alabama. Predicted dispersal locations include areas where the southern phenotype of I. scapularis dominates, suggestive of a possible mechanism for previously described unidirectional gene flow from north to south. In addition, the model demonstrates that three species-specific songbird traits - breeding range, migration timing, and propensity for tick attachment - each play a major role in the relative magnitude of tick dispersal by different songbird species. The pattern of I. scapularis dispersal predicted by this model suggests that migrating songbirds may have contributed to the range expansion of the tick historically, and may continue to do so presently and into the future, particularly as climate changes the geographic areas that are suitable for I. scapularis. Ultimately, widespread tick dispersal by migrating songbirds likely increases the human risk of Lyme disease and other tick-borne diseases in the United States.