Sexual size dimorphism (SSD) can strongly influence the evolution of reproductive strategies and life history. If SSD is extreme, and other characters (e.g., genitalic size) also increase with size, then functional conflicts may arise between the sexes. Spiders offer an excellent opportunity to investigate this issue because of their wide range of SSD. By using modern phylogenetic methods with 16 species of orb-weaving spiders, we provide strong evidence for the “positive genitalic divergence” model, implying that sexual genitalic dimorphism (SGD) increases as SSD increases. This pattern is supported by an evolutionary mismatch between the absolute sizes of male and female genitalia across species. Indeed, our findings reveal a dramatic reversal from male genitalia that are up to 87× larger than female genitalia in size-monomorphic species to female genitalia that are up to 2.8× larger in extremely size-dimorphic species. We infer that divergence in SGD could limit SSD both in spiders, and potentially in other taxa as well. Further, male and female body size, as well as male and female genitalia size, are decoupled evolutionarily. Finally, we show a negative scaling (hypoallometry) of male and female genitalic morphology within sexes. Evolutionary forces specific to each sex, such as larger female size (increased fecundity) or smaller male size (enhanced mate-searching ability), may be balanced by stabilizing selection on relative genitalic size.