Discovering the mutational events that fuel adaptation to environmental change remains an important challenge for evolutionary biology. The classroom example of a visible evolutionary response is industrial melanism in the peppered moth (Biston betularia): the replacement, during the Industrial Revolution, of the common paletypicaform by a previously unknown black (carbonaria) form, driven by the interaction between bird predation and coal pollution1. Thecarbonarialocus has been coarsely localized to a 200-kilobase region, but the specific identity and nature of the sequence difference controlling thecarbonaria-typicapolymorphism, and the gene it influences, are unknown2. Here we show that the mutation event giving rise to industrial melanism in Britain was the insertion of a large, tandemly repeated, transposable element into the first intron of the genecortex. Statistical inference based on the distribution of recombinedcarbonariahaplotypes indicates that this transposition event occurred around 1819, consistent with the historical record. We have begun to dissect the mode of action of thecarbonariatransposable element by showing that it increases the abundance of acortextranscript, the protein product of which plays an important role in cell-cycle regulation, during early wing disc development. Our findings fill a substantial knowledge gap in the iconic example of microevolutionary change, adding a further layer of insight into the mechanism of adaptation in response to natural selection. The discovery that the mutation itself is a transposable element will stimulate further debate about the importance of ‘jumping genes’ as a source of major phenotypic novelty3.