Abstract Amongst other factors, host behaviour critically determines the patterns with which blood parasites occur in wild host populations. In particular, migratory hosts that sequentially occupy distant sites within and across years are expected to show distinct patterns of blood parasitism depending on their population-specific schedules and whereabouts. Here, we monitored haemosporidian parasitism in two populations of European bee-eaters (Merops apiaster), breeding in Portugal and Germany, with fundamentally different spatiotemporal migration patterns and colonisation histories. We describe and compare the composition of their parasite fauna as well as host population-, age- and sex-specific patterns in the frequency and intensity of infections. We found haemosporidian prevalence to be higher in Portugal compared with Germany and the prevalence generally increased with host age in both populations. Bee-eaters breeding in Portugal and wintering in western Africa mostly hosted parasites of the genus Haemoproteus, while Plasmodium lineages prevailed in birds breeding in Germany and wintering in central Africa. We found 18 genetic lineages, of which nine uniquely occurred in Germany, three uniquely in Portugal and six occurred in both breeding populations. The infection intensities (= % infected per inspected erythrocytes) ranged from 0.002% up to maximally 2.5% in Portugal and 9.6% in Germany. The intensity was higher in Germany compared with Portugal, vastly varied between the parasite genera (Haemoproteus > Plasmodium), but also differed between lineages of the same genus. Our results suggest that populations from different parts of a host’s breeding range differ in prevalence and the composition of their haemosporidian assemblages, rather than in the intensity of their infections. Whether these patterns are mainly caused by differential habitat use throughout the annual cycle and/or the population-specific co-evolutionary backgrounds of a host species in range expansion remains to be elucidated.