Chaperonins are multi-subunit double-ring complexes that mediate the folding of nascent or denatured proteins. Gene duplication has been a potent force in the evolution of chaperonins in Archaea. Here we show that gene conversion has also been an important factor. We utilized a novel maximum likehood-based phylogenetic method for scanning DNA sequence alignments for regions of anomalous phylogenetic signal, such as those affected by gene conversion. Our results suggest that in crenarchaeotes, where an ancient gene duplication producing alpha and beta subunits took place in the common ancestor of the Pyrodictium, Aeropyrum, Pyrobaculum and Sulfolobus lineages, multiple independent gene conversions have occurred between the alpha and beta genes independently in each of these groups. Significantly, the conversions have repeatedly homogenized the region of the gene encoding the substrate-binding domain. This suggests that while the alpha and beta subunits in crenarchaeotes share only 50-60% overall amino acid sequence identity, they do not possess distinct roles in the binding of substrate. Cryptic gene conversion between distantly related paralogs may be more common than is currently appreciated, and could be a significant factor in slowing the functional differentiation of proteins encoded by duplicate genes long after their duplication.