We examined temporal and geographical distribution of Haemoproteus sp. and Plasmodium sp. parasites in Swedish willow warblers, Phylloscopus trochilus. Parasite lineages were detected with molecular methods in 556 birds from 41 sites distributed at distances up to 1,500 km. Two mitochondrial lineages of Haemoproteus sp. were detected, WW1 in 56 birds and WW2 in 75 birds, that differed by 5.2% sequence divergence. We discuss the reasons behind the observed pattern of variation and identify 3 possible causes: (1) variation in the geographic distribution of the vector species, (2) the degree of parasite sharing with other bird species coexisting with the willow warbler, and (3) timing of transmission. Our results support a fundamental and rarely tested assumption of the now classical Hamilton–Zuk hypothesis of sexual selection, namely, that these parasites vary in both time and space. Such fluctuations of parasites and the selection pressure they supposedly impose on the host population are likely to maintain variation in immune system genes in the host population.