The study of model organisms on islands may shed light on rare long-range dispersal events, uncover signatures of local evolutionary processes, and inform demographic inference on the mainland. Here, we sequenced the genomes ofArabidopsis thalianasamples from the oceanic island of Madeira. These samples include the most diverged worldwide, likely a result of long isolation on the island. We infer that colonization of Madeira happened between 70 and 85 ka, consistent with a propagule dispersal model (of size ≥10), or with an ecological window of opportunity. This represents a clear example of a natural long-range dispersal event inA. thaliana. Long-term effective population size on the island, rather than the founder effect, had the greatest impact on levels of diversity, and rates of coalescence. Our results uncover a selective sweep signature on the ancestral haplotype of a known translocation in Eurasia, as well as the possible importance of the low phosphorous availability in volcanic soils, and altitude, in shaping early adaptations to the island conditions. Madeiran genomes, sheltered from the complexities of continental demography, help illuminate ancient demographic events in Eurasia. Our data support a model in which two separate lineages ofA. thaliana, one originating in Africa and the other from the Caucasus expanded and met in Iberia, resulting in a secondary contact zone there. Although previous studies inferred that the westward expansion ofA. thalianacoincided with the spread of human agriculture, our results suggest that it happened much earlier (20–40 ka).