The study of genital diversity has experienced rapidly burgeoning attention over the past few decades. This research has shown that male genitalia in internally fertilizing animals exhibit remarkably rapid and complex evolution. In recent years, a consensus has emerged that sexual selection is responsible for much of the observed genital diversity, with natural selection largely playing a subsidiary role. Despite enhanced understanding of the key proximate forms of selection responsible for genital evolution, we still have a poor grasp of the broader, ultimate causes and consequences of the striking diversity of genitalia. Here, we highlight three topics that have so far received comparatively little attention and yet could prove critically important. First, we encourage investigation of ecology's direct and indirect roles in genital diversification, as ecological variation can influence selection on genitalia in several ways, perhaps especially by influencing the context of sexual selection. Second, we need more research into the effects of genital divergence on speciation, as genital differences could enhance reproductive isolation through either a lock-and-key process (where selection directly favors reproductive isolation) or as an incidental by-product of divergence. Third, we echo recent calls for increased research on female genitalia, as non-trivial female genital diversity exists, and multiple mechanisms can lead to rapid diversification of female genitalia. For all three topics, we review theory and empirical data, and describe specific research approaches for tackling these questions. We hope this work provides a roadmap toward increased understanding of the causes and consequences of the conspicuous diversity of primary sexual traits, and thus toward new insights into the evolution of complex traits and the phenotypic causes of speciation.