The evolutionary enlightened management of species with complex life cycles often requires the development of mathematical models integrating demographic and genetic data. The genetic structure of the endangered European eel (Anguilla anguilla L.) has been thoroughly analyzed in several studies in the past years. However, the interpretation of the key demographic and biologic processes that determine the observed spatio-temporal genetic structure has been very challenging owing to the complex life cycle of this catadromous species. Here, we present the first integrated demographic-genetic model applied to the European eel that explicitly accounts for different levels of larval and adult mixing during oceanic migrations and allows us to explore alternative hypotheses on genetic differentiation. Our analyses show that (i) very low levels of mixing occurring during larval dispersal or adult migration are sufficient to erase entirely any genetic differences among sub-populations; (ii) small-scale temporal differentiation in recruitment can arise if the spawning stock is subdivided in distinct reproductive groups; and (iii) the geographic differentiation component might be overestimated if a limited number of temporal recruits are analyzed. Our study can inspire the scientific debate on the interpretation of genetic structure in other species characterized by complex life cycle and long-range migrations.