Birds possess the most diverse assemblage of haemosporidian parasites, although the true diversity is unknown due to high genetic diversity and insufficient sampling across all avian clades. Waterfowl (Order Anseriformes) are an ideal group to discover hidden parasite diversity and examine the role of host ecology in parasite transmission. Waterfowl contain 2 distinct feeding guilds, dabbling and diving, which differ in niche utilization that likely alters vector encounter rates and haemosporidian parasite risk. To determine the role of feeding guild in haemosporidian parasitism we analysed 223 blood samples collected by hunters from the upper Midwest of the United States from 2017 to 2019. Fifty-four individuals were infected by haemosporidian parasites (24·2% prevalence). Infection prevalence differed significantly between dabbling (34·9%, n = 109) and diving (14·0%, n = 114) ducks. Feeding guild was the only host trait that could predict haemosporidian infection risk, with a significantly higher risk in dabbling ducks. Twenty-four haemosporidian lineages were identified, with 9 identified for the first time. Thirteen lineages were found only in dabbling ducks, 5 only in diving ducks and 6 in both feeding guilds. Community analysis showed that each feeding guild harboured a unique parasite community. There was no phylogenetic signal of feeding guild within a phylogenetic reconstruction of North American waterfowl haemosporidian lineages. Our results demonstrate that waterfowl contain a diverse and distinct community of haemosporidian parasites. The unique composition of each feeding guild determines not only haemosporidian infection risk but also community structure. This is the first report of such an impact for waterfowl feeding guilds.