Generalist parasites experience selective pressures from the various host species they infect. However, it is unclear if parasite transmission among host species precludes the establishment of host-specific adaptations and population genetic structure. We assessed the population genetic structure of the vector-transmitted avian haemosporidian parasite Haemoproteus majoris (lineage WW2; n = 34 infections) in a single site in southern Sweden among 10 of its host species. The 2 best-sampled host genera were Phylloscopus (2 species, n = 15 infections) and Sylvia (4 species, n = 15). We designed a sequence capture protocol to isolate 1.13 Mbp (ca. 5%) of the parasite genome and identified 1399 variable sites among the sequenced infections. In a principal components analysis, infections of Phylloscopus and Sylvia species mostly separated along the first 2 principal components. Sites with the highest FST values between the genera were found in genes that have mostly not been implicated in infection pathways, but several sites code for amino acid changes. An analysis of molecular variance confirmed significant variation among host genera, but not among host species within genera. The distribution of Tajima’s D among sequenced loci was negatively skewed, plausibly reflecting a history of bottleneck followed by population expansion. Tajima’s D was lower in infections of Phylloscopus than Sylvia, plausibly because WW2 began infecting Phylloscopus hosts after it was already a parasite of Sylvia hosts. Our results provide evidence of vector-transmitted parasite population differentiation among host species in a single location. Future work should focus on identifying the mechanisms underlying this genetic population structure.