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Unlike other European countries, the human population genetics and demographic history of Metropolitan France is surprisingly understudied. In this work, we combined newly genotyped samples from various zones in France with publicly available data and applied both allele frequency and haplotype-based methods to describe the internal structure of this country, using genome-wide single nucleotide polymorphism (SNP) array genotypes. We found out that French Basques, already known for their linguistic uniqueness, are genetically distinct from all other groups and that the populations from southwest France (namely the Gascony region) share a large proportion of their ancestry with Basques. Otherwise, the genetic makeup of the French population is relatively homogeneous and mostly related to Southern and Central European groups. However, a fine-grained, haplotype-based analysis revealed that Bretons slightly separated from the rest of the groups, due mostly to gene flow from the British Isles in a time frame that coincides both historically attested Celtic population movements to this area between the 3th and the ninth centuries CE, but also with a more ancient genetic continuity between Brittany and the British Isles related to the shared drift with hunter-gatherer populations. Haplotype-based methods also unveiled subtle internal structures and connections with the surrounding modern populations, particularly in the periphery of the country., Funding was provided by the Agencia Estatal de Investigación and Fondo Europeo de Desarollo Regional (FEDER) (grant CGL2016-75389-P), Agència de Gestió d’Ajuts Universitaris i de la Recerca (Generalitat de Catalunya) Grant 2014SGR2866, and “Unidad de Excelencia María de Maeztu”, funded by the MINECO (ref: MDM-2014–0370). SAB was supported by the Agencia Estatal de Investigación FPI grant BES-2014–069224.