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Cultivated (Citrullus lanatus var. lanatus) and citron type (var. citroides) watermelon collected from different areas on the African continent are remarkably diverse in fruit and seed morphology. Chloroplast DNA investigations using PCR-RFLP and sequencing analysis of several non-coding regions were conducted to infer their biogeographic and evolutionary relationships, origin and domestication history. Variability within C. lanatus was observed at regions of high A + T content, resulting in indels and transversions mainly. Distinct chlorotype lineages were identified separating the cultivated and egusi-type watermelon from var. citroides accessions. This suggests an ancient split from a common ancestor and haplotype fixation. Three haplotypes as a result of relatively recent indel events were detected within var. citroides. The geographical range of two of the main citroides haplotypes is relatively similar across southern Africa. Accessions with the most ancient citroides haplotype originated in Swaziland and South Africa resulting in colonization routes from this area all over the world. Chloroplast divergence is not associated with morphological divergence. The cultivated and wild watermelon appear to have diverged independently from a common ancestor, possibly C. ecirrhosus from Namibia.