Monkeypox is an emerging zoonosis endemic to Central and West Africa. Monkeypox virus (MPXV) is genetically structured in two major clades (clades 1 and 2/3), but its evolution is poorly explored. We show that the population transmitted in West Africa (clades 2/3) experienced limited drift. Conversely, clade 1 (transmitted in the Congo Basin) possibly underwent a bottleneck or founder effect. Depending on the model used, we estimated that the two clades separated ∼560-860 (HPD: 450-960) years ago, a period characterized by expansions and contractions of rainforest areas, possibly creating the ecological conditions for the MPXV reservoir(s) to migrate. In the Congo Basin, MPXV diversity is characterized by four subpopulations that show no geographic structuring. Conversely, clades 2/3 are spatially structured with two populations located West and East of the Dahomey Gap. The distinct histories of the two clades may derive from differences in MPXV ecology in West and Central Africa.