Rapid life-history changes caused by size-selective harvesting are often interpreted as a response to direct harvest selection against a large body size. However, similar trait changes may result from a harvest-induced relaxation of natural selection for a large body size via density-dependent selection. Here, we show evidence of such density-dependent selection favouring large-bodied individuals at high population densities, in replicated pond populations of medaka fish. Harvesting, in contrast, selected medaka directly against large-bodied medaka and, in parallel, decreased medaka population densities. Five years of harvesting were enough for harvested and unharvested medaka populations to inherit the classically-predicted trait differences, whereby harvested medaka grew slower and matured earlier than unharvested medaka. We demonstrate that this life-history divergence was not driven by direct harvest selection for a smaller body size in harvested populations, but by density-dependent natural selection for a larger body size in unharvested populations.