Hosts have developed and evolved defense strategies to limit parasite damage. Hosts can reduce the damage that parasites cause by decreasing parasite fitness (resistance) or without affecting parasite fitness (tolerance). Because a parasite species can infect multiple host species, determining the effect of the parasite on these hosts and identifying host defense strategies can have important implications for multi‐host–parasite dynamics. Over 2 years, we experimentally manipulated parasitic flies (Protocalliphora sialia) in the nests of tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis). We then determined the effects of the parasites on the survival of nestlings and compared defense strategies between host species. We compared resistance between host species by quantifying parasite densities (number of parasites per gram of host) and measured nestling antibody levels as a mechanism of resistance. We quantified tolerance by determining the relationship between parasite density and nestling survival and blood loss by measuring hemoglobin levels (as a proxy of blood recovery) and nestling provisioning rates (as a proxy of parental compensation for resources lost to the parasite) as potential mechanisms of tolerance. For bluebirds, parasite density was twice as high as for swallows. Both host species were tolerant to the effects of P. sialia on nestling survival at their respective parasite loads but neither species were tolerant to the blood loss to the parasite. However, swallows were more resistant to P. sialia compared to bluebirds, which was likely related to the higher antibody‐mediated immune response in swallow nestlings. Neither blood recovery nor parental compensation were mechanisms of tolerance. Overall, these results suggest that bluebirds and swallows are both tolerant of their respective parasite loads but swallows are more resistant to the parasites. These results demonstrate that different host species have evolved similar and different defenses against the same species of parasite.