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Abstract TheAdelges(Dreyfusia)piceae(Ratzeburg) species complex is a taxonomically unstable group of six species. Three of the species are cyclically parthenogenetic [Ad.nordmannianae(Eckstein),Ad.prelli(Grossmann), andAd.merkeri(Eichhorn)] and three are obligately asexual [Ad.piceae,Ad.schneideri(Börner), andAd.nebrodensis(Binazzi & Covassi)]. Some species are high‐impact pests of fir (Abies) trees, so stable species names are needed to communicate effectively about management. Therefore, to refine species delimitation, guided by a reconstruction of their biogeographic history, we genotyped adelgids from Europe, North America, and the Caucasus Mountains region with 19 microsatellite loci, sequenced the COI DNA barcoding region, and compared morphology. Discriminant analysis of principal components of microsatellite genotypes revealed four distinct genetic clusters. Two clusters were morphologically consistent withAd.nordmannianae. One of these clusters consisted of samples from the Caucasus Mountains and northern Turkey, and the other included samples from this region as well as from Europe and North America, whereAd.nordmannianaeis invasive. A third cluster was morphologically consistent withAd.piceae, and included individuals from Europe, where it is native, and North America, where it is invasive. In North America, the majority ofAd.piceaeindividuals were assigned to two geographically widespread clones, suggesting multiple introductions. The fourth cluster included individuals morphologically consistent withAd.prelliorAd.merkeri. However, based on genetic assignments, hybrid simulations, and approximate Bayesian computation, we find it likely that these are contemporary hybrids betweenAd.nordmannianaeandAd.piceaethat arose independently in Europe and North America, so we propose thatAd.prelliandAd.merkeriare invalid. Finally, we synonymiseAd.schneideri(syn.n.)withAd.nordmannianaeand designateAd.nebrodensisas subspeciesAd.piceae nebrodensis(stat.n.). Our revised taxonomy therefore recognises two species:Ad.nordmannianaeandAd.piceae, which we estimate to have diverged recently, during one of the last two interglacial periods. Finally, we comment on this species complex being in the midst of transition between sexual and asexual reproduction, a pattern that is probably common in Adelgidae.