Spatial variation in the occurrence of browsing ungulates can drive local adaptation in plant traits but also lead to trade-offs among traits potentially enhancing competitive ability versus resistance or tolerance to browsing. Plectritis congesta populations co-occurring on islands with and without ungulates offer striking examples of population-level variation in traits, such as plant height and fruit morphology, which may also affect fitness. We monitored split-plot common gardens exposed to and protected from browsing ungulates for 5 yr to test for local adaptation (local vs. foreign comparison) in P.congesta by comparing the survival and fecundity of 4,392 sown fruits from six island populations where ungulates were present ("historically exposed") and six where they were absent ("historically naïve"). Our results indicate that local adaptation to browsing in P.congesta favored rosette formation, delayed flowering, reduced height, and the production of wingless fruits, all of which appeared to enhance survival, fecundity, and population growth in plants from populations historically exposed to ungulate browsers, as compared to plants from historically naïve populations. In contrast, plants from historically naïve populations displayed higher relative fitness in the absence of ungulates, increased in height, flowered earlier, and produced fewer but larger, winged fruits, often in large terminal inflorescences. Our results support the hypothesis that variation in the occurrence of ungulate browsers has led to (1) spatial heterogeneity in natural selection and rapid adaptation in P.congesta populations on islands, and (2) context-dependent trade-offs in the fitness value of traits linked to the resistance or tolerance of browsing versus success in competition for light, pollinators, or other resources. Because patterns of selection in plant communities will vary with the introduction or extirpation of top predators or browsers, we suggest historical context, local adaptation, and the capacity for rapid adaptation should be a focal concern of those aiming to maximize or predict population persistence under environmental change in conservation plans.