Drosophila melanogaster has been an historically important system for investigating the genetic basis of longevity, and will continue to be valuable as new technologies permit genomic explorations into the biology of aging. The utility of D. melanogaster resides in two resources: its powerful genetic tools as a model system, and a natural ecology that provides substantial genetic variation across significant environmental heterogeneity. Here we provide a review of the genetics of longevity in D. melanogaster, in which we describe the characterization of individual aging genes, the complexity of the genetic architecture of this quantitative trait, and the evaluation of natural genetic variation in the evolution of life histories.