Understanding how hosts minimize the cost of emerging infections has fundamental implications for epidemiological dynamics and the evolution of pathogen virulence. Despite this, few experimental studies in natural populations have tested whether, in response to disease emergence, hosts evolve resistance, which reduces pathogen load through immune activation, or tolerance, which limits somatic damages without decreasing pathogen load. Further, none has done so accounting for significant natural variation in pathogen virulence, despite known effects on host responses to infection. Here, we investigate whether eastern North American house finches (Haemorrhous mexicanus) have evolved resistance and/or tolerance to their emerging bacterial pathogen, Mycoplasma gallisepticum. To do so, we inoculated finches from disease-exposed and disease-unexposed populations with 55 distinct isolates of varying virulence. First, although peak pathogen loads, which occurred ~8 days post-inoculation, did not differ between experimentally-inoculated finches from disease-exposed versus unexposed population, pathogen loads subsequently decreased faster and to a greater extent in finches from exposed populations. These results suggest that finches from exposed populations are able to clear the infection through adaptive immune processes. Second, however, finches from exposed populations also displayed lower symptom severity for a given pathogen load, suggesting that a damage-limitation mechanism, or tolerance, has accompanied the evolution of immune clearance. Our results highlight that resistance and tolerance should be seen as complementary, not alternative, defence strategies: the evolution of resistance benefits from the concomitant evolution of tolerance mechanisms that protect against the damage of immune activation, while the evolution of tolerance without resistance will risk runaway selection on pathogen virulence.