Taphrinomycotina is the smallest subphylum of the phylum Ascomycota. It is an assemblage of distantly related early diverging lineages of the phylum, comprising organisms with divergent morphology and ecology; however, phylogenomic analyses support its monophyly. In this study, we report the isolation of a yeast strain, which could not be assigned to any of the currently recognised five classes of Taphrinomycotina. The strain of the novel budding species was recovered from extra virgin olive oil and characterised phenotypically by standard methods. The ultrastructure of the cell wall was investigated by transmission electron microscopy. Comparisons of barcoding DNA sequences indicated that the investigated strain is not closely related to any known organism. Tentative phylogenetic placement was achieved by maximum-likelihood analysis of the D1/D2 domain of the nuclear LSU rRNA gene. The genome of the investigated strain was sequenced, assembled, and annotated. Phylogenomic analyses placed it next to the fission  Schizosaccharomyces  species. To accommodate the novel species,  Novakomyces olei , a novel genus  Novakomyces , a novel family Novakomycetaceae, a novel order Novakomycetales, and a novel class Novakomycetes is proposed as well. Functional analysis of genes missing in  N. olei  in comparison to  Schizosaccharomyces pombe  revealed that they are biased towards biosynthesis of complex organic molecules, regulation of mRNA, and the electron transport chain. Correlating the genome content and physiology among species of Taphrinomycotina revealed some discordance between pheno- and genotype.  N. olei  produced ascospores in axenic culture preceded by conjugation between two cells. We confirmed that  N. olei  is a primary homothallic species lacking genes for different mating types.