Summary The domestic pigeon’s exceptional phenotypic diversity was key in developing Darwin’s Theory of Evolution and establishing the concept of artificial selection in domestic species. However, unlike its domestic counterpart, its wild progenitor, the rock dove Columba livia , has received considerably less attention. Therefore, questions regarding their domestication, evolution, taxonomy, and conservation status remain unresolved. We generated whole-genome sequencing data from 65 historical rock dove samples representing all currently recognised subspecies and spanning the species’ original geographic distribution. Our dataset includes three specimens from Darwin’s collection and the type specimens of five different taxa. We characterised rock doves’ population structure, genomic diversity and gene-flow patterns. We show the West African subspecies C. l. gymnocyclus is basal to rock doves and domestic pigeons. Our results show gene-flow signals between the rock dove’s sister species C. rupestris and all rock doves except the West African populations. Our results led us to propose an evolutionary model for the rock dove considering the Pleistocene refugia theory. We propose that today’s rock dove genetic diversity and introgression patterns derive from a history of allopatric cycles and dispersion waves during the Quaternary glacial and interglacial periods. To explore the rock dove domestication history, we combined our new dataset with available genomes from domestic pigeons. Our results point to at least one domestication event in the Levant region that gave rise to all domestic breeds analysed in this study. Finally, we propose a species-level taxonomic arrangement to reflect the evolutionary history of the West African rock dove populations.

Redefining rock doves,Columba livia, using historical whole genome sequences