Plant defense strategies against pathogen attack can be divided into either resistance or tolerance. Variation in tolerance is expressed as differences in the relationship between host fitness (or yield) and the degree of infection. Plant tolerance of pathogen attack remains poorly understood both in terms of its specific mechanisms and in terms of the evolutionary processes by which it has arisen. Theoretical models predict that it is the result of coevolution between host and pathogen, suggesting greater tolerance in interactions with native as opposed to introduced pathogens. Therefore, we quantified and compared the degree of tolerance expressed in the interaction of Senecio vulgaris with the rust fungus Coleosporium tussilginis, which is native to the UK, and the introduced rust fungus Puccinia lagenophorae. We used the reaction norm approach to quantify tolerance and its components. The S. vulgaris-C. tussilaginis interaction expressed a significantly greater degree of tolerance, as reductions in host growth and fitness per unit infection were significantly less than with P. lagenophorae. The key mechanism for this greater tolerance to C. tussilaginis was a significantly smaller reduction in photosynthesis per unit infection than with P. lagenophorae, at both leaf and whole plant scales. There was no significant difference in the relationship between whole plant photosynthesis and host reproduction. We discuss these responses in the context of coevolution for tolerance in host-pathogen interactions.