Peripheral populations (i.e., those occurring on the edge of a species’ distribution range) can have different origins and genetic characteristics, and they may be critical for conservation of genetic diversity. We investigated European peripheral populations of Scrophularia arguta, a widespread, annual plant distributed from Arabia to Northwest Africa and Macaronesia. Only two small disjunct population groups of this species occur in Europe, specifically in West‐Central and Southeast Iberia. To disclose the origin of these populations and determine their importance for conservation of S. arguta genetic diversity, we analysed DNA sequences from two nuclear and two plastid regions and AFLP markers in populations sampled mainly across the western distribution range of the species, and modelled the species distribution under present and late Quaternary conditions. The analyses revealed the presence of three distinct lineages of S. arguta in Europe, as a result of multiple colonisation waves at different times in the Quaternary. Two of these lineages, occurring in Southeast Iberia, are the result of more or less recent dispersal from Northwest Africa. In contrast, West‐Central Iberian populations are strongly differentiated from the remaining range of S. arguta, and can be considered as peripheral relict populations. Our study is the first to demonstrate the occurrence of at least three colonisations of the European continent from Africa by a native plant species. The diverse histories and genetic makeup of resulting populations confirm the importance of peripheral populations, and particularly of ancient relict populations, for conservation of global genetic diversity in widespread species.