Understanding factors that influence the spatial and temporal distributions of blood parasites is important to help predict how host species and their parasites may respond to global change. Factors that may influence parasite distributions are land cover and host dispersal patterns, which may result in exposure of a host to novel parasites, or escape from parasites of their origin. We screened golden-winged warblers from across the United States and Canada for blood parasites, and investigated whether land-use patterns or host dispersal affected the prevalence and composition of haemosporidian assemblages. Parasite prevalence varied strongly with study area, and areas with high agricultural cover had a significantly higher prevalence of Leucocytozoon and Parahaemoproteus parasites. Lineages of Parahaemoproteus and Leucocytozoon were genetically differentiated among study areas, and prevalence and composition of parasite assemblages indicated an increase in parasite prevalence and accumulation of unique parasite lineages from the southeast to the northwest. This matches the historical range expansion and natal dispersal patterns of golden-winged warblers, and suggests that golden-winged warblers may have been sensitive to novel parasites as they dispersed. The high prevalence and diversity of parasite lineages in the north-west extent of their breeding range (Manitoba) indicates that this population may face unique pressures.