Background: Recent intensive efforts to control malaria in African countries expose vector populations to additional adaptive challenges. The main malaria mosquitoes of the continent display an array of adaptive strategies to cope with such challenges. The development of genomic resources will empower genetic studies that are crucial to understand the evolutionary history and adaptive potential of these vectors. Methodology/Principal findings: Here we constructed double-digest Restriction Associated DNA (ddRAD) libraries and generated 6461 Single Nucleotide Polymorphisms (SNPs) that we used to explore the population structure and demographic history of wild-caught Anopheles moucheti from Cameroon. The genome-wide distribution of allelic frequencies among sampled populations best fitted that of an old population at equilibrium, characterized by a weak genetic structure and extensive genetic diversity, presumably due to a large long term effective population size. In contrast to other important African malaria vectors, polymorphic chromosomal inversions play little role in the genome architecture and evolutionary adaptation of An. moucheti. Conclusions/Significance: Our study provides the first investigation of the genetic structure and diversity in An. moucheti at the genomic scale. Despite a weak genetic structure and absence of adaptive divergence, the adaptive potential of this mosquito remains significant owing to a great diversity and standing genetic variation that can be used to face current vector control measures and other rapid anthropogenic and environmental changes.