A conceptual divide exists between ecological and evolutionary approaches to understanding adaptive radiation, although the phenomenon is inherently both ecological and evolutionary. This divide is evident in studies of phytophagous insects, a highly diverse group that has been frequently investigated with the implicit or explicit goal of understanding its diversity. Whereas ecological studies of phytophagous insects increasingly recognize the importance of tri-trophic interactions as determinants of niche dimensions such as host-plant associations, evolutionary studies typically neglect the third trophic level. Here we attempt to reconcile ecological and evolutionary approaches through the concept of the ecological niche. We specifically present a tri-trophic niche concept as a foil to the traditional bi-trophic niche concept for phytophagous insects. We argue that these niche concepts have different implications for understanding herbivore community structure, population divergence, and evolutionary diversification. To this end, we offer contrasting empirical predictions of bi- and tri-trophic niche concepts for patterns of community structure, the process of population divergence, and patterns of evolutionary diversification of phytophagous insects.