The geographic structuring of parasite communities across the range of a single host species can illuminate patterns of host-population connectivity. To determine the location of parasite transmission in a Neotropical migrant bird species, we sampled adult and hatch-year (HY) birds across the breeding and wintering range of the Swainson's thrush (SWTH), an abundant passerine with a migratory divide. We examined the phylogenetic relationships among cytochrome b lineages of the avian blood parasite genera Haemoproteus, Plasmodium, and Leucocytozoon and determined the transmission location of unique lineages. We found that Haemoproteus and Plasmodium lineages are transmitted on California breeding grounds, whereas Leucocytozoon transmission occurs on Alaskan breeding grounds. The presence of hemosporidians on wintering grounds and shared lineages between the SWTH and resident species suggests that transmission of some of these lineages occurs on both breeding and wintering grounds. We emphasize that the sampling of HY birds and local resident heterospecifics will supplement vector studies to determine the key players in hemosporidian host switching and range-expansion events.