The biotic and the abiotic environment play a major role in shaping plant phenotypes and their geographic distributions. However, little is known about the extent to which plant phenotypes match local patterns of herbivory across fine-grained habitat mosaics, despite the strong effect of herbivory on plant fitness. Through a reciprocal transplant-common garden experiment with clonally propagated rhizomes, we tested for local phenotypic differentiation in bittercress (Brassicaceae: Cardamine

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... ifolia ) plants collected across an ecotonal habitat mosaic. We found that bittercress in sunny meadows (high herbivory) and shaded understories (low herbivory) have diverged in heritable growth and herbivore resistance phenotypes. The expression of these differences was habitat dependent, mirroring patterns of adaptive divergence in phenotypic plasticity between plant populations in meadow and understory habitats at broader geographic scales, and showed no evidence for a constraint imposed by growth-defense tradeoffs. Most notably, plants derived from shade habitats exhibited a weaker shade-induced elongation response (i.e., shade avoidance syndrome, SAS) and reduced resistance to herbivory, relative to plants derived from sun habitats, when both were grown in shade common gardens. Greenhouse experiments revealed that divergent SAS phenotypes in shade conditions were expressed in offspring grown from seed as well. Finally, we observed partially non-overlapping flowering phenology between habitat-types in the field, which may be at least one factor that helps to reinforce habitat-specific phenotypic divergence. Altogether, our study illuminates how a native plant may cope with overlapping biotic and abiotic stressors across a fine-grained habitat mosaic.