Developmental plasticity provides individuals with a distinct advantage when the reproductive environment changes dramatically. Variation in population density, in particular, can have profound effects on male reproductive success. Females may be easier to locate in dense populations, but there may be a greater risk of sperm competition. Thus, males should invest in traits that enhance fertilization success over traits that enhance mate location. Conversely, males in less dense populations should invest more in structures that will facilitate mate location. In Lepidoptera, this may result in the development of larger antennae to increase the likelihood of detecting female sex pheromones, and larger wings to fly more efficiently. We explored the effects of larval density on adult morphology in the gum-leaf skeletoniser moth, Uraba lugens, by manipulating both the number of larvae and the size of the rearing container. This experimental arrangement allowed us to reveal the cues used by larvae to assess whether absolute number or density influences adult responses. Male investment in testes size depended on the number of individuals, while male investment in wings and antennae depended upon larval density. In contrast, the size of female antennae and wings were influenced by an interaction of larval number and container size. This study demonstrates that male larvae are sensitive to cues that may reveal adult population density, and adjust investment in traits associated with fertilization success and mate detection accordingly.