This study presents extensive molecular phylogenetic and morphometric data for Anoplocephaloides dentata (Galli-Valerio, 1905)-like cestodes (Anoplocephalidae) and related species parasitizing arvicoline rodents (voles and lemmings) in the Holarctic region. The molecular phylogeny is based on nucleotide sequences of cytochrome oxidase I (mtDNA) and 28S ribosomal RNA. Anoplocephaloides dentata-like cestodes included three main clades, two in western Eurasia and one in the Holarctic region (excluding western Eurasia). Three well-supported sublineages were included in the southern European clade, one of which represents the true A. dentata from Chionomys nivalis and sympatric Microtus arvalis and Dinaromys bogdanovi. These clades generally had non-overlapping distributions and showed a preference for certain host species. Multivariate analysis of morphometric data failed to discriminate unambiguously the various A. dentata-like lineages recovered in the molecular phylogeny, although two to three of the (sub) lineages were morphologically divergent. The overall evidence suggests, however, that instead of a single host-generalist species there are at least five more or less host-specific species of A. dentata-like cestodes. Colonization of new host lineages seems to have been the predominant mode of diversification, suggested by the considerable incongruence between host and parasite phylogenies at multiple taxonomic levels. Based on the results of the molecular survey, a redescription and neotype designation are provided for A. dentata.