The genetic structure of a collection of more than 2900 unique genotypes representative of both the cultivated and the wild grapevine gene pools was studied with the help of nuclear neutral and non-neutral molecular markers. The subgroups obtained through complementary clustering methods were matched with their geographic origins and their phenotypic characterizations. The main clustering obtained with microsatellite markers on the larger genotype dataset, was confirmed by the SNP variation of 80 genes of reference, chosen as the most informative ones out of a total of 960 genes, re-sequenced on a subset of representative genotypes (corecollection). The partition of diversity of both neutral and non-neutral markers pointed to patterns that could be related to historical processes of domestication, selection and breeding, and to geography, from ancestral groups derived from opposite regions of the grapevine distribution area, down to a number of subgroups linked to specific local uses and grape features, finally merging into a family level. Within the cultivated compartment, the three most significant subgroups corresponded to the wine grapes from the Western Europe, the wine grapes from Balkans and Central Europe, and the table grapes from the East. A further subdivision evidenced family or sub-regional structures, such as the groupings of grapevines from Maghreb, from the Italian and the Iberian peninsula, from Russia and the Caucasian region, or the Muscat, the Savagnin and the Pinot-Gouais families. The study of the relationships with the wild compartment revealed that the cultivated gene pool was derived from two separate wild grapevine gene pools, one wild pool from the East that contributed to the table grapes, and a second wild pool from West Europe that contributed to the wine grapes. Presenting the more complete dataset to date, this work allows researchers to precisely account for genetic structure when sampling diversity within unstructured groups, as it is required by modern methods of genome-wide association genetics. It also adds a layer of information to the already documented national grapevine collection of Vassal, France, confirming its role as a reference for grapevine genetic studies.