Generalist and specialist parasites are predicted to trade off transmission efficiency with host virulence, depending on host range. However, very few empirical studies test this trade-off in parasites at both ends of this spectrum simultaneously. Here, we examine parasitaemia (as a proxy for transmission efficiency) and virulence (assessed through 2 metrics of host immunity) in birds infected by a generalist lineage of Haemoproteus, comparing these with birds infected by more specialist Haemoproteus lineages, and birds uninfected by any haemoparasite. We compared the same metrics for specialist-infected birds, depending on whether a species was a ‘usual’ host or ‘spillover’ host. Immune metrics of specialist-infected birds did not differ from those of uninfected birds, but generalist-infected birds had elevated heterophil:lymphocyte (H:L) ratios and elevated white blood cell (WBC) counts compared to both other groups. Parasitaemia of specialist lineages was nearly 5 times higher than that of generalist lineages. Moreover, specialist-infected spillover hosts had higher H:L ratios and higher WBC counts compared to usual hosts for these lineages, with parasitaemia nearly 10 times lower in spillover hosts compared to usual hosts, although sample sizes of spillover hosts are, by definition, small. Our data provide support for the evolution of tolerance in specialist host-parasite interactions, with increased transmission efficiency for the parasite and reduced impacts on the host.