AbstractHost–parasite dynamics often vary over time, brought about by changes in the parasite’s virulence or the host’s ability to resist or tolerate the parasite. Although virulence evolution in microparasites is well studied, we know little about temporal change in the pathogenicity of macroparasites such as blood‐feeding insects. Using data collected over 35 yr, we report a reduction in pathogenicity of the hematophagous swallow bug (Cimex vicarius) on its Cliff Swallow (Petrochelidon pyrrhonota) host. Relative to experimentally fumigated, parasite‐free nests, the negative effects of bugs on nestling swallow body mass and survival were less in the later years of the study than in the earlier years, and the negative relationship between nestling body mass and bug abundance became weaker over time. The survival of adult birds exposed to swallow bugs increased throughout the study, while survival of birds from parasite‐free nests decreased over time. Swallow bug abundance per nest, bug body size, and bug age ratios did not change during the study. Between‐colony transmission of bugs showed less immigration into larger colonies than in earlier studies, but there was no net change in transmission. Cliff Swallows did not reduce their exposure to bugs over time by being more likely to avoid infested nest or colony sites. Parents increased the number of food deliveries to their offspring over time in the presence of parasites, but the total amount of food delivered was unchanged. The reduced cost of swallow bug ectoparasitism does not seem related to changes in parasite narrow‐sense virulence, the host’s avoidance of parasites, the presence of alternative hosts for bugs, or climate‐driven phenological mismatches. The results probably reflect the Cliff Swallow’s evolving of greater tolerance to swallow bugs, brought about by the bird’s shift from natural cliff nesting sites to artificial structures that may harbor more bugs than natural cliffs. This study shows that hosts can respond relatively rapidly to high levels of parasitism, and provides support for models that suggest the evolution of tolerance should be expected in some host–parasite systems.