The plant stress and plant vigour hypotheses are competing paradigms pertaining to the preference and performance of herbivorous insects on their host plants. Tests of these hypotheses ideally require detailed information on aspects of soil nutrition, foliar nutrient levels and parameters of herbivore fitness, but such studies are uncommon. These hypotheses were tested using the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), reared on its host plant, Brassica napus (L.), grown in an experimental system of five nutrient regimes. Different levels of fertilizer treatments significantly affected the nutrient content of B. napus foliage and this in turn affected the preference and performance of P. xylostella. Ovipositing females discriminated among host plants grown in soils subjected to different fertilizer treatments and selected plants on which pre-imaginal survival was highest, development fastest and longevity of the next generation of adults the longest, even when food was scarce. Plants subjected to herbivory by P. xylostella responded by producing elevated levels of some nutrients (e.g., sulphur), but other nutrient levels declined in infested leaves (e.g., nitrogen). Regardless of the rate of fertilizer application, plants compensated for herbivory by increasing root mass compared to un-infested control plants; plants grown in soils receiving the optimum quantity of fertilizer developed the most robust root systems when infested. The plant stress and the plant vigour hypotheses are likely to be at the opposite ends of a continuum of responses between insects and their host plants. Our investigations indicate a complex set of interactions involving both bottom-up and top-down effects, which interact to affect host plant quality, oviposition site selection by female herbivores and the fitness of their offspring.