The origins of phenotypic variation within mimetic Heliconius butterflies have long fascinated biologists and naturalists. However, the evolutionary processes that have generated this extraordinary diversity remain puzzling. Here we examine intraspecific variation across Heliconius cydno diversification and compare this variation to that within the closely related H. melpomene and H. timareta radiations. Our data, which consist of both mtDNA and genome scan from nearly 2250 AFLP loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that likely diverged from H. melpomene during the Pliocene-Pleistocene boundary. MtDNA suggest that this radiation originated in Central America or the Northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome-scan data indicate significant admixture among sympatric H. cydno/H.timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno color pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms.