We used both nuclear ribosomal genes (28S rDNA, 18S rDNA, 5.8S rDNA, internal transcribed spacer regions: ITS1, ITS2) and mitochondrial CO1 sequences to group or distinguish morphotypes of Parafavella, a problematic genus of tintinnid ciliates of the marine microzooplankton. We sequenced 30 single cells of Parafavella from the Bering Sea, the Greenland Sea, and the East/Japan Sea. Sequences were obtained from 4 morphotypes, typically ascribed to P. gigantea, P. greenlandica, P. jorgenseni, and P. subrotundata and from GenBank, the nuclear ribosomal genes of P. parumdentata were retrieved. Cells of the five morphotypes had identical 18S and 5.8S gene sequences. ITS1, ITS2 and 28S sequences produced two clusters: one grouping P. greenlandica and P. parumdentata and the other grouping P. jorgenseni, P. gigantea, and P. subrotundata. In contrast, CO1 nucleotide data yielded eight haplotypes clustered into five groups: one composed of P. greenlandica morphotypes, two distinct haplotypes of P. jorgenseni, and two distinct haplotypes of P. gigantea with one including P. subrotundata morphotypes. We investigated the co‐occurrence of different morphotypes in samples from sites across a large gradient of latitude and concentrations of Parafavella cells. Natural communities contained 2–6 different morphotypes. We conclude that both crypticity and polymorphism characterize Parafavella, as known for other tintinnid genera.