Rift Valley Fever is an acute zoonotic viral disease caused by Rift Valley Fever virus (RVFV) that affects ruminants and humans in Sub-Saharan Africa and the Arabian Peninsula. We used phylogenetic analyses to understand the demographic history of RVFV populations, using sequence data from the three minigenomic segments of the virus. We used phylogeographic approaches to infer RVFV historical movement patterns across its geographic range, and to reconstruct transitions among host species. Results revealed broad circulation of the virus in East Africa, with many lineages originating in Kenya. Arrival of RVFV in Madagascar resulted from three major waves of virus introduction: the first from Zimbabwe, and the second and third from Kenya. The two major outbreaks in Egypt since 1977 possibly resulted from a long-distance introduction from Zimbabwe during the 1970s, and a single introduction took RVFV from Kenya to Saudi Arabia. Movement of the virus between Kenya and Sudan, and CAR and Zimbabwe, was in both directions. Viral populations in West Africa appear to have resulted from a single introduction from Central African Republic. The overall picture of RVFV history is thus one of considerable mobility, and dynamic evolution and biogeography, emphasizing its invasive potential, potentially more broadly than its current distributional limits.