Environmental manipulations have consistently demonstrated a cost of reproduction in the capital-breeding seed beetle, Callosobruchus maculatus, as females deprived of seeds or mates lay fewer eggs and thereby increase their longevity. Yet fecundity and longevity tend to be positively correlated within populations, perhaps as a consequence of individual differences in resource acquisition. We conducted a split-brood experiment that combined a manipulation of seed availability (seeds present or absent) with a quantitative-genetic analysis of fecundity and lifespan in each environment. Each trait was significantly heritable in each environment. Seed availability not only altered mean fecundity and longevity between environments, but also modified how the traits were correlated within environments. The signs of both the phenotypic and genetic correlations switched from positive when seeds were present to negative when seeds were absent. This reversal persisted even after the effect of body mass (a potential indicator of resource acquisition) was statistically controlled. Cross-environment genetic correlations were positive but significantly less than one for each trait. We suggest that the reversal of the fecundity-longevity relationship depends on a shift in the relative importance of resource-acquisition and resource-allocation loci between environments. In particular, a cost of reproduction may be apparent at the individual level only when seeds are scarce or absent because differences in reproductive effort become large enough to overwhelm differences in resource acquisition. Despite their common dependence on resources acquired during larval stages, fecundity and lifespan in C. maculatus do not appear to be tightly coupled in a physiological or genetic sense.