Immune system components differ in their functions and costs, and immune defense profiles are likely to vary among species with differing ecologies. We compared adaptive immune defenses in two closely related species that have contrasting inflammatory immune responses, the widespread and abundant house sparrow (Passer domesticus) and the less abundant tree sparrow (Passer montanus). We found that the house sparrow, which we have previously shown mounts weaker inflammatory responses, exhibits stronger adaptive immune defenses, including antibody responses, natural antibody titers, and specific T-cell memory, than the tree sparrow. Conversely, tree sparrows, which mount strong inflammatory responses, also mount stronger nonspecific inflammatory T-cell responses but weaker specific adaptive responses. Prevalence of avian malaria parasite infections, which are controlled by adaptive immune defenses, was higher in the geographically restricted tree sparrow than in the ubiquitous house sparrow. Together these data describe distinct immune defense profiles between two closely related species that differ greatly in numbers and distributions. We suggest that these immunological differences could affect fitness in ways that contribute to the contrasting abundances of the two species in North American and Western Europe.