The genus Aporrectodea includes some of the most conspicuous earthworm species, but its taxonomic history is among the most complex within the family Lumbricidae. Molecular phylogenetic studies have produced some advances by assigning former Aporrectodea species to other monophyletic clades and by detecting species level lineages within the cosmopolitan caliginosa-trapezoides complex. However, little attention has been devoted to endemic taxa of Aporrectodea such as Ap. rubra, Ap. arverna, Ap. gogna, Ap. balisa, Ap. velox, Ap. giardi voconca and Ap. longa ripicola. These earthworms (and additional populations of Ap. longa and Ap. nocturna) were included in a molecular phylogenetic framework in order to reconstruct the ancestral range of the genus, as well as to help understand its diversification within its native range and to perform a systematic revision. Species delimitation, ancestral area reconstruction and Bayesian inference of the phylogenetic relationships were performed using a large gene sequence (COI) dataset and a narrower dataset composed of 5 mitochondrial and nuclear markers. Phylogenetic position and species delimitation indicated that Ap. giardi voconca and Ap. longa ripicola constitute species-level entities not closely related to Ap. giardi or Ap. longa, and they were thus redescribed as Aporrectodea voconca stat. nov. and Aporrectodea ripicola stat. nov. Ancestral area reconstruction enabled location of the origin of Aporrectodea in the Auvergne-Rhône-Alps, in Southeastern France. The study findings provide some insight into the evolution of functional traits in this ecologically successful genus. Ap. rubra and Ap. arverna (small, reddish, epigeic/epianecic) and Ap. gogna (very large, dark, anecic) were recovered as the earliest branching taxa, suggesting a complex evolution of functional traits within this genus.