The response of herbivorous insects to plant drought stress can range from positive to negative, and it has been challenging to understand the causes of this variation. We tested whether plant trait values associated with aridity gradients might underlie this variation and how effects vary among two insect feeding guilds.  Here we propose that plants trait values associated with adaptation to arid environments would result in positive effects of experimental drought on herbivores, with such plant species adaptively shifting resources away from resistance to maintain performance under stress. In contrast, plant with trait values associated with adaptation to mesic environments would result in negative effects of drought because such species lose vigor and thus decline in their host-quality. We tested these predictions using experimental manipulations in 13 milkweed species (genus Asclepias) adapted to a wide range of environmental conditions, and herbivore performance of a specialist leaf-chewer (monarch butterfly; Danaus plexippus) and sap-feeder (oleander aphid; Aphis nerii). We exposed plants to species-specific watering regimes physiologically calibrated to maximize (100%) or reduce (50%) stomatal conductance and then monitored the performance of the herbivores. The effects of drought stress on herbivore survival ranged from strongly positive (50% increase) to strongly negative (80% decrease) among milkweed species, but these effects were inconsistent between the two herbivores.  We demonstrated that the indirect effects of drought on herbivores varied tremendously among closely related plant species and between co-occurring insect herbivores.