Members of Amphidinium Claparède and Lachmann constitute a major part of sand-dwelling benthic dinoflagellates worldwide. The genus is traditionally defined by its small epicone size, not exceeding one third of the total cell length. It has long been suspected that this functional definition does not reflect phylogeny, yet the problem of identifying the type species A. operculatum and closely related species has until now hindered attempts to redefine the genus. In this study 12 Amphidinium species were examined using phylogenetic analyses based on nuclear-encoded, partial, large subunit (LSU) rDNA, with a further six Amphidinium species being included in a morphological cladistic analysis. The species selected represented taxa with a range of morphological dissimilar epicone forms. Both cladistic analysis and analyses based on partial LSU rDNA revealed that Amphidinium species with minute left-deflected epicones formed a monophyletic clade that included the type species. Amphidinium species with other epicone types were found to be unrelated to this clade. The type species A. operculatum was identified based on general cell shape and size, position of a dark organelle previously defined as a stigma, and origin of the sulcus. The description of A. elegans by Grell and Wohlfarth-Bottermann was found to be identical to it. A species fitting the original description of A. operculatum was cultured and included in the analyses. Based on cladistic and molecular analyses, it grouped together with all other species with minute left-deflected epicones, and this group constitutes the true genus Amphidinium sensu stricto. An emendation of the genus definition is presented.