Ongoing speciation in most African malaria vectors gives rise to cryptic populations, which differ remarkably in their behaviour, ecology and capacity to vector malaria parasites. Understanding the population structure and the drivers of genetic differentiation among mosquitoes is critical for effective disease control because heterogeneity within species contribute to variability in malaria cases and allow fractions of vector populations to escape control efforts. To examine the population structure and the potential impacts of recent large-scale control interventions, we have investigated the genomic patterns of differentiation in mosquitoes belonging to the Anopheles nili group, a large taxonomic group that diverged ~3-Myr ago. Using 4343 single nucleotide polymorphisms (SNPs), we detected strong population structure characterized by high FST values between multiple divergent populations adapted to different habitats within the Central African rainforest. Delineating the cryptic species within the Anopheles nili group is challenging due to incongruence between morphology, ribosomal DNA and SNP markers consistent with incomplete lineage sorting and/or interspecific gene flow. A very high proportion of loci are fixed (FST = 1) within the genome of putative species, which suggests that ecological and/or reproductive barriers are maintained by strong selection on a substantial number of genes.