The nucleotide sequences of the complete or nearly complete mitochondrial (mt) genomes of seven vetigastropods were determined: Angaria neglecta (Angarioidea), Phasianella solida (Phasianelloidea), Granata lyrata (Seguenzioidea), Tegula lividomaculata and Bolma rugosa (Trochoidea), Diodora graeca (Fissurelloidea) and Lepetodrilus schrolli (Lepetodriloidea). While the mt genomes of the superfamilies Angarioidea, Phasianelloidea, Seguenzioidea and Trochoidea conform generally to the ancestral gene order of Vetigastropoda and Gastropoda, those of the superfamilies Fissurelloidea and Lepetodriloidea have suffered important rearrangements. The gene order of the mtDNA of Chrysomallon squamiferum, a representative of Neomphalina, was also analysed since it has been proposed to be closely related to Vetigastropoda, and showed a distinct arrangement. The reconstructed phylogenies recovered Neomphalina as a distinct gastropod lineage that is the sister group (only with moderate bootstrap support) of a clade including Vetigastropoda and Neritimorpha + Caeno‐gastropoda while the relative position of Heterobranchia and Patellogastropoda in the gastropod tree could not be determined definitively due to their long branches. Within the monophyletic Vetigastropoda, the superfamily Fissurelloidea was recovered as the sister group of two lineages, one including Lepetodriloidea as the sister group of Seguenzioidea + Halitoidea, the other including Phasianelloidea, Angarioidea and Trochoidea without resolved relationships. The long branches of Fissurelloidea were found to introduce significant tree instability in phylogenetic reconstruction. The new phylogeny supports that the loss of the right pallial gill occurred multiple times in vetigastropod evolution as previously suggested and that Phasianelloidea, Angarioidea and Trochoidea radiated from a common asymmetric (single‐gilled) ancestor that lived in the middle Palaeozoic.