In the ciliate Tetrahymena thermophila, regulated secretion of peptides occurs from dense core granules named mucocysts. Prior work from our laboratory revealed that mucocyst biogenesis depends on several proteins associated with lysosomes and lysosome-related organelles, namely cathepsins and VPS10/sortilins. To identify additional factors required in this pathway, we have used whole genome sequencing to analyze a recessive Mendelian mutant, called UC616, that is defective in mucocyst biogenesis. In an F2 mutant pool derived by outcrossing and then backcrossing UC616, we identified a homozygous single nucleotide variant predicted to alter a splice junction within a Tetrahymena homolog of the VPS8 gene, which we call TtVPS8a. The mutation in TtVPS8a indeed inhibits intron excision and introduces a premature stop codon in the N-terminal domain of the protein. Importantly, the mucocyst biogenesis defect in UC616 can be fully rescued by endogenous-level expression of a full length, GFP-tagged copy of TtVPS8a. Yeast VPS8 encodes a subunit of CORVET, a complex shown to mediate vesicle tethering in the endolysosomal system in yeast and mammals. In UC616, mucocysts are absent and a protein that forms the wildtype mucocyst core instead accumulates in heterogeneous cytoplasmic compartments. Interestingly, T. thermophila and related ciliates have multiple paralogs of VPS8 and other CORVET-complex subunits, while lacking subunits that are specific to the related HOPS complex in fungi and animals. Tetrahymena maintains several distinct organelles, in addition to mucocysts, which appear related to lysosomes, and our results suggest that specialized paralogous CORVET tethering complexes may play an important role in their biogenesis. Our results also highlight the accessibility of this organism to forward genetic approaches, to interrogate this and other pathways.