The heterotrophic Crypthecodinium cohnii is a major model for dinoflagellate cell biology, and a major industrial producer of docosahexaenoic acid, a key nutraceutical and added pharmaceutical compound. Despite these factors, the family Crypthecodiniaceae is not fully described, which is partly attributable to their degenerative thecal plates, as well as the lack of ribotype-referred morphological description in many taxons. We report here significant genetic distances and phylogenetic cladding that support inter-specific variations within the Crypthecodiniaceae. We describe Crypthecodinium croucheri sp. nov. Kwok, Law and Wong, that have different genome sizes, ribotypes, and amplification fragment length polymorphism profiles when compared to the C. cohnii. The interspecific ribotypes were supported by distinctive truncation-insertion at the ITS regions that were conserved at intraspecific level, indicating stabilization. The long genetic distances between Crypthecodiniaceae and other dinoflagellate orders support the separation of the group, which includes related taxons with high oil content and degenerative thecal plates, to be ratified to the order level. The current study provides the basis for future specific demarcation-differentiation, which is an important facet in food safety, biosecurity, sustainable agriculture feeds, and biotechnology licensing of new oleaginous models.