It has long been recognized that interspecific hybridization is common in plants, enhancing processes of diversification and speciation. With the widespread utilization of molecular tools, interspecific hybridization – as revealed through incongruence among two or more phylogenetic data sets – is now inferred to be even more prevalent than indicated by morphological and cytogenetic evidence. Using Gossypium as an example, we show how multiple molecular markers have implicated a high frequency of historical hybridization between lineages whose modern descendants are strongly isolated by geography and intrinsic genetic barriers. For example, transoceanic dispersal of propagules from Africa to the New World led to the creation of a novel allotetraploid lineage, as well as the introgression of African repetitive elements into a Mexican diploid species. By mechanisms that remain obscure, fully one-quarter of modern Gossypium species appear to have experienced historical interspecific cytoplasmic and possibly nuclear introgression. These remarkable observations of interspecific genetic exchange emerge from a genus for which such contact would appear improbable, implying that historical hybridization is a more creative force than suspected in angiosperm evolution.