The study of genital diversity has experienced rapidly burgeoning attention over the past few decades. This research has centered on internally fertilizing animals, where male genitalia often show remarkably rapid and elaborate evolution. In recent years, a consensus has emerged that sexual selection and sexual conflict are responsible for most of the observed genital diversity, with natural selection playing a subsidiary role. Despite this major advance in understanding the key forms of selection primarily responsible for genital evolution, we still have a poor understanding of the broader causes and consequences of the striking diversity of genitalia. Here, we plot a course forward for a more complete understanding of genital evolution, highlighting three topics that have so far received comparatively little attention and yet could prove critically important. First, we echo the recent calls for increased research on female genitalia, as non-trivial female genital diversity exists, and 5 major mechanisms can lead to its rapid diversification. Second, we encourage more investigation of ecology’s direct and indirect roles in genital diversification, as ecological variation can influence selection on genitalia in many ways, perhaps especially through its frequent alterations of the context of sexual selection. Third, we direly need more research into the effects of genital divergence on speciation, as genital differences could often enhance reproductive isolation through either a lock-and-key process or as an incidental by-product of divergence. For each topic, we review theory and empirical data, and describe specific research approaches for tackling these outstanding questions. We hope we are on the verge of gaining crucial new insights into the causes and consequences of the conspicuous diversity of animal genitalia.