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Phylogenetic relationships in the genus Cortinarius with emphasis on European species were studied by integrating a molecular phylogenetic analysis of nuclear rDNA sequences with morphological, chemical, and ecological data. Internal transcribed spacers (ITS1 and ITS2, including 5.8S) and the D1–D2 regions of nuclear rDNA of 262 Cortinarius species including most of the recognised subgenera from Europe, South America, Australia, Tasmania, New Zealand, and Asia were sequenced and analysed by maximum likelihood and neighbour joining. Our morphological and molecular analyses showed considerable disagreement with earlier morphology-based hypotheses concerning the infrageneric delimitations in Cortinarius. We propose a new base for a more natural classification system in Cortinarius involving the taxonomic rearrangement of the species into the following major lineages that we informally designate as “clades” at this time: (1) phlegmacioid species are included in Alluti, Amarescentes, Arguti, Calochroi, Caerulescentes, Percomes, Phlegmacioides, Phlegmacium, Purpurascentes, Scauri, and Vulpini; (2) the Heterocliti clade includes species of the subgenera Leprocybe and Cystogenes ; (3) most of the Myxacium species are included in the Delibuti and Myxacium clades; (4) part of Rozites are included in the Rozites clade; (5) the north-hemispheric species of subgenus Dermocybe are included in the Dermocybe clade and part of the south-hemispheric species in the Splendidi clade; (6) part of Sericeocybe are integrated in the Anomali and Telamonia clades; (7) members of subgenus Cortinarius are assigned to the Cortinarius clade; (8) telamonioid taxa are included in the Obtusi, Renidentes, and Telamonia clades. Several Cortinarius species with peculiar patterns of morphology and basidiome coloration had isolated positions in the sequence analysis, and the evolutionary relationships among the major lineages remained unresolved. Our results suggest the convergent evolution of certain morphological traits across phylogenetically divergent lineages in Cortinarius. However, combinations of features such as pileipellis anatomy, spore shape, veil coloration, basidiome pigments, and stipe shape appear useful to circumscribe clades. Our molecular phylogenetic analysis allows insights in global geographical patterns of species distribution within the major lineages in the genus Cortinarius. The clade structure proposed here could be used as backbone for further more detailed systematic studies.