Polyploid formation and processes that create partial genomic duplication generate redundant genomic information, whose fate is of particular interest to evolutionary biologists. Different processes can lead to diversification among duplicate genes, which may be counterbalanced by mechanisms that retard divergence, including gene conversion via nonreciprocal homoeologous exchange. Here, we used genomic resources in diploid and allopolyploid cotton (Gossypium) to detect homoeologous single nucleotide polymorphisms provided by expressed sequence tags from G. arboreum (A genome), G. raimondii (D genome) and G. hirsutum (AD genome), allowing us to identify homoeo-single nucleotide polymorphism patterns indicative of potential homoeologous exchanges. We estimated the proportion of contigs in G. hirsutum that have experienced nonreciprocal homoeologous exchanges since the origin of polyploid cotton 1-2 million years ago (Mya) to be between 1.8% and 1.9%. To address the question of when the intergenomic exchange occurred, we assayed six of the genes affected by homoeo-recombination in all five Gossypium allopolyploids using a phylogenetic approach. This analysis revealed that nonreciprocal homoeologous exchanges have occurred throughout polyploid divergence and speciation, as opposed to saltationally with polyploid formation. In addition, some genomic regions show multiple patterns of homoeologous recombination among species.