The genetic architecture of variation in adult lifespan was examined for a population of recombinant inbred lines, each of which had been crossed to both inbred parental strains from which the lines were derived, after emergence from both high and low larval density. QTL affecting lifespan were mapped within each sex and larval density treatment by linkage to highly polymorphic roo transposable element markers, using a composite interval mapping method. We detected a total of six QTL affecting lifespan; the additive effects and degrees of dominance for all were highly sex- and larval environment-specific. There were significant epistatic interactions between five of the lifespan QTL, the effects of which also differed according to genetic background, larval density and sex. Five additional QTL were identified that contributed to differences among lines in their sensitivity to variation in larval density. Further fine-scale mapping is necessary to determine whether candidate genes affecting lifespan that are included in the regions to which the QTL map are actually responsible for the observed variation in lifespan.