Reproduction shortens lifespan in practically all organisms examined so far, but the underlying mechanisms remain largely unknown to date. Here I review what evolutionary and molecular biologists have learned about such "costs of reproduction" in the fruit fly (Drosophila melanogaster) since Maynard Smith's (1958) seminal discovery that sterile mutants in D. subobscura live substantially longer than fertile wildtype flies. Together with observations from the nematode worm (Caenorhabditis elegans) and other organisms, the data from Drosophila suggest that there are at least four general principles that underlie trade-offs between reproduction and lifespan: (1) trade-offs between survival and reproduction are widespread; (2) the relationship between increased lifespan and decreased fecundity can be uncoupled under certain conditions; (3) while survival costs of reproduction might not necessarily be due to competitive resource allocation, we lack robust alternative explanations for their occurrence; and (4) physiological trade-offs between reproduction and longevity do not always translate into evolutionary genetic trade-offs. I conclude that - despite much recent progress - our current understanding of the proximate basis of survival costs of reproduction remains very limited; much future work on the genetics and physiology of such trade-offs will be required to uncover their mechanistic basis.