Adaptive developmental plasticity has been demonstrated across a number of taxa in response to variables such as photoperiod, resource abundance, and predator presence. Demographics also vary temporally and spatially within populations, but few studies have examined the possibility that developmental plasticity in response to changes in these variables can alter phenotypic distributions. Plastic responses to variable population density and sex ratio may play an important role in explaining phenotypic variation in nature. In this study, we examine two species of spiders (Nephila plumipes and Argiope keyserlingi) to examine whether there is evidence that males alter their development in response to demographics in natural populations. We studied spiders in which developing males can use pheromones as a cue of the density of conspecific males and females. We used published information about the mating systems and life history of each species to make predictions about expected patterns of plasticity in development time and correlated changes in adult body size in response to demographic variation. Within each species, male size and mass were positively correlated with the density of males but negatively correlated with the density of females, and as predicted, this was true only when calculated at spatial scales relevant to selection in each species. In contrast, seasonal variation in photoperiod could not explain measured variance in male size. Our results support the idea that developmental plasticity in response to demographics has a significant effect on phenotypic distributions in natural populations. Our results suggest that a proportion of variation in male phenotypes could be explained as a plasticity-mediated evolutionary response to variation in population demographics rather than as a physiological response to resource abundance and/or photoperiod.