Phenotypically plastic responses have been increasingly documented in response to intraspecific, behavioral (often sexual) signals such as mating calls. We explored the effect of short-term exposure to male calling song on a reproductive life history trade-off in adult females of the wing dimorphic cricket species, Gryllus firmus. In G. firmus, long-winged females possess flight muscles and small ovaries immediately after the adult molt, whereas short-winged females possess small, non-functional flight muscles and large ovaries at the same age. In long-winged females, flight muscles are histolyzed during ovary growth that occurs after the adult molt. Because of these differences in reproductive physiology, we predicted different responses to calling song exposure between the two morphs. We hypothesized that such exposure would boost ovary growth in both wing morphs, but also increase flight muscle histolysis in long-winged females, producing a greater relative response to exposure in this morph. As expected, we saw a significant increase in ovary mass in exposed females of both morphs, and a greater relative response in long-winged females. Calling song exposure did not have a strong effect on flight muscle histolysis, suggesting that the relatively larger ovary response in long-winged females was perhaps fueled instead by reallocation of flight fuels. Our study documents the rapid adult response of a fitness-linked trait to the adult social environment, a result with far-reaching implications, as the experience of mating signals during adulthood should be nearly universal across species.