Although natural selection often varies across ontogeny, it remains unclear what conditions enable selection in one life-cycle stage to shape evolution in others. Organisms that undergo metamorphosis are useful for addressing this topic because, despite the dramatic life-history transition that separates their highly specialized life-cycle stages, the stages only exhibit evolutionary independence in some cases. Using a comparative study of dragonflies, we examined three conditions that are hypothesized to allow selection in one stage to affect evolution in others. First, contrary to predictions that life-cycle stages in lineages with less dramatic metamorphoses (e.g. hemimetabolous insects) do not evolve independently, we found that the evolution of larval body shape is not affected by selection on adult shape. Next, supporting the hypothesis that homologous and/or co-adapted structures do not evolve independently, selection for larger wings are associated with the evolution of a functionally co-adapted larval trait, the sheaths that store developing wing tissue. Finally, consistent with expectations of minimal stage-specific evolution in traits linked to a single biochemical pathway, species with more wing melanization have evolved weaker larval melanin immune defenses. Thus, even in organisms that undergo metamorphosis, some kinds of traits may have greater capacity for stage-specific evolution than others.