The mimetic butterflies Heliconius erato and Heliconius melpomenehave undergone parallel radiations to form a near-identical patchworkof over 20 different wing-pattern races across the Neotropics.Previous molecular phylogenetic work on these radiations has suggestedthat similar but geographically disjunct color patterns arosemultiple times independently in each species. The neutral markersused in these studies, however, can move freely across color patternboundaries, and therefore might not represent the history ofthe adaptive traits as accurately as markers linked to color patterngenes. To assess the evolutionary histories across different loci, wecompared relationships among races within H. erato and within H.melpomene using a series of unlinked genes, genes linked to colorpattern loci, and optix, a gene recently shown to control red colorpatternvariation.We found that although unlinked genes partitionpopulations by geographic region, optix had a different history,structuring lineages by red color patterns and supporting a singleorigin of red-rayed patterns within each species. Genes closelylinked (80–250 kb) to optix exhibited only weak associations withcolor pattern. This study empirically demonstrates the necessity ofexamining phenotype-determining genomic regions to understandthe history of adaptive change in rapidly radiating lineages. Withthese refined relationships, we resolve a long-standing debateabout the origins of the races within each species, supporting thehypothesis that the red-rayed Amazonian pattern evolved recentlyand expanded, causing disjunctions of more ancestral patterns.