The Batesian mimetic swallowtail butterfly Papilio dardanus exhibits numerous distinct wing colour morphs whose evolutionary origins require large phenotypic shifts. A phylogenetic framework to study the history of these morphs was established by DNA sequencing of representative subspecies from sub-Saharan Africa and Indian Ocean islands. Two mitochondrial genes and the nuclear internal transcribed spacer marker revealed deeply separated eastern and western African mainland lineages, plus one lineage each on Madagascar and Grande Comore. These markers showed very little polymorphism within lineages. In contrast, markers genetically linked to the mimicry locus H, including the transcription factor invected and two adjacent amplified fragment length polymorphisms-derived sequences, showed high nucleotide diversity but were not geographically structured. Variation in the unlinked wingless gene showed a similar pattern, rejecting the hypothesis that high level of variation in the H region is due to balancing selection exerted by the phenotypes. The separation from a common ancestor with Papilio phorcas estimated at 2.9 Ma coincides with the origin of a mimicry model, Danaus chrysippus. However, the model reached Africa only at the time of the internal splits of P. dardanus mtDNA groups, here estimated at 0.55–0.94 Ma. The nuclear genome shows less geographic structure and may not track recent population differentiation, suggesting that widespread mimicry morphs have arisen early in the evolution of the P. dardanus lineage, although after the male–female dimorphism which is ancestral. The current wide distribution of P. dardanus and population subdivision evident from mtDNA may have been achieved only with the spread of the models across Africa.