The cost of adaptations may depend on environmental conditions. We consider how the fitness cost of resistance to the herbicide triazine in Amaranthus hybridus interacts with folivory from the beetle Disonycha glabrata. Triazine-resistant (TR) genotypes suffer a fitness cost because of a pleiotropic reduction in the light reaction of photosynthesis, which in turn often leads to a reduction in photosynthetic rate. We found that the fitness cost of triazine resistance was 360% greater in the presence than absence of D. glabrata. This resulted from multiple phenotypic trade-offs, with TR plants suffering greater herbivory and displaying a diminished tolerance of damage. Our work highlights the importance of incorporating appropriate ecological variation into the assessment of fitness trade-offs. The results of this study also illustrate the potential for herbivores to impose selection on photosynthetic variation, and for variation in resource acquisition to obscure fitness costs.