Drosophilid fruit flies have provided science with striking cases of behavioural adaptation and genetic innovation. A recent example is the invasive pest Drosophila suzukii, which, unlike most other Drosophila, lays eggs and feeds on undamaged, ripening fruits. This poses a serious threat for fruit cultivation, but also offers an interesting model to study evolution of behavioural innovation. We developed genome and transcriptome resources for D. suzukii. Coupling analyses of these data with field observations, we propose a hypothesis of the origin of its peculiar ecology. Using nuclear and mitochondrial phylogenetic analyses, we confirm its Asian origin, and reveal a surprising sister relationship between the eugracilis and the melanogaster subgroups. While the D. suzukii genome is comparable in size and repeat content to other Drosophila species, it has the lowest nucleotide substitution rate among the species analysed in this study. This finding is compatible with the overwintering diapause of D. suzukii, which results in a reduced number of generations per year compared to its sister species. Genome-scale relaxed clock analyses support a late Miocene origin of D. suzukii, concomitant with paleogeological and climatic conditions that suggest an adaptation to temperate montane forests, a hypothesis confirmed by field trapping. We propose a causal link between the ecological adaptations of D. suzukii in its native habitat and its invasive success in Europe and North America.