Increasing promiscuity within populations is generally predicted to 1) reduce the opportunity for males to monopolise females, and thus potentially weaken male pre-copulatory sexual selection and 2) to generate post-copulatory sexual selection via sperm competition and cryptic female choice. However, a lack of ability to experimentally manipulate promiscuity levels within populations has hampered progress in directly testing these predictions. Moreover, traditional measures of the strength of sexual selection, such as the Bateman gradient (the correlation between the number of mates and number of offspring), only capture pre-copulatory, but not post-copulatory, sexual selection. To address these issues we genetically manipulated female sexual receptivity in Drosophila melanogaster and generated hyper-promiscuous populations. Increased promiscuity resulted in a significantly reduced male Bateman gradient, but no change in the female Bateman gradient. Using multivariate analyses – which include effects of paternity share and mate fecundity – we reveal that the primary force of sexual selection on males changes from pre-copulatory in control populations, to post-copulatory in hyper-promiscuous populations. Our results therefore provide an experimental demonstration that promiscuity has sex-specific effects on the strength of sexual selection, and mediates a switch from pre- to post-copulatory selection in males.