When hosts have a long coevolutionary history with their parasites, fitness costs of chronic infection have often been assumed to be negligible. Yet, experimental manipulation of infections sometimes reveals effects of parasites on their hosts, particularly during reproduction. Whether these effects translate into fitness costs remains unclear. Here, we present the results of an experimental study conducted in a free-ranging population of red-winged blackbirds (Agelaius phoeniceus) naturally experiencing a high prevalence of haemosporidian infections, with > 95% of breeding adults infected with parasites from one or more haemosporidian genus. To assess effects of infection during reproduction, we manipulated adult red-winged blackbird females’ parasite burden by administering an anti-haemosporidian medication before onset of egg-laying. Experimental reduction of infection resulted in significant benefits to mothers and their offspring. Medicated females laid heavier clutches, invested more in incubation and provisioning behaviour, and produced more fledglings than control females. Nestlings of medicated females had higher haematocrit, higher blood glucose, and lower reactive oxygen metabolites than nestlings of control females. Overall, our results provide evidence that, even in a species with a long history of high prevalence of infection, parasites can lead to decreased maternal investment and offspring quality, substantially reducing fitness.