The emergence of agriculture in West-Central Africa approximately 5,000 years ago, profoundly modified the cultural landscape and mode of subsistence of most sub-Saharan populations. How this major innovation has had an impact on the genetic history of rainforest hunter-gatherers-historically referred to as 'pygmies'-and agriculturalists, however, remains poorly understood. Here we report genome-wide SNP data from these populations located west-to-east of the equatorial rainforest. We find that hunter-gathering populations present up to 50% of farmer genomic ancestry, and that substantial admixture began only within the last 1,000 years. Furthermore, we show that the historical population sizes characterizing these communities already differed before the introduction of agriculture. Our results suggest that the first socio-economic interactions between rainforest hunter-gatherers and farmers introduced by the spread of farming were not accompanied by immediate, extensive genetic exchanges and occurred on a backdrop of two groups already differentiated by their specialization in two ecotopes with differing carrying capacities.