Rapid genitalia evolution is believed to be mainly driven by sexual selection. Recently, noncopulatory genital functions have been suggested to exert stronger selection pressure on female genitalia than copulatory functions. In bedbugs (Cimicidae), the impact of the copulatory function can be isolated from the noncopulatory impact. Unlike in other taxa, female copulatory organs have no function in egg-laying or waste-product expulsion. Males perform traumatic mating by piercing the female integument, thereby imposing antagonistic selection on females and suspending selection to morphologically match female genitalia. We found the location of the copulatory organ evolved rapidly, changing twice between dorsal and ventral sides, and several times along the anteroposterior and the left–right axes. Male genital length and shape varied much less, did not appear to follow the positional changes seen in females, and showed no evidence for coevolution. Female genitalia position evolved 1.5 times faster than male genital length and shape and showed little neutral or geographic signals. Instead, we propose that nonmorphological male traits, such as mating behavior, may drive female genitalia morphology in this taxon. Models of genitalia evolution may benefit from considering morphological genital responses to nonmorphological stimuli, such as male mating behavior or copulatory position.