Two major ecological transitions marked the history of the Black Sea after the last Ice Age. The first was the postglacial transition from a brackish-water to a marine ecosystem dominated by porpoises and dolphins, once this basin was reconnected back to the Mediterranean Sea (ca. 8,000 years B.P.). The second occurred during the last decades, when overfishing and hunting activities brought these predators close to extinction, deeply impacting the structure and dynamics of the ecosystem. Estimating the extent of this decimation is essential for characterizing this ecosystem's dynamics and for formulating restoration plans. However this extent is poorly documented in historical records. We addressed this issue for one of the main Black Sea predators, the harbor porpoise, using a population genetics approach. Analyzing its genetic diversity using an Approximate Bayesian Computation approach, we show that only a demographic expansion (at most 5,000 years ago) followed by a contemporaneous population collapse can explain the observed genetic data. We demonstrated that both the postglacial settlement of harbor porpoises in the Black Sea and the recent anthropogenic activities have left a clear footprint on their genetic diversity. Specifically, we inferred a strong population reduction (~90%) that occurred within the last five decades, which can therefore clearly be related to the recent massive killing of small cetaceans and to the continuing incidental catches in commercial fisheries. Our study thus provides a first quantitative assessment of these demographically catastrophic events, while also showing that two separate historical events can be inferred from contemporary genetic data.