BACKGROUND: The BBSome is an octameric protein complex crucial for ciliary transport, though it also participates in multiple other cellular processes. These diverse functions may result from the co-option of its ancestral roles. Studying the BBSome in flagellated protists can provide insights into these ancestral functions and their subsequent adaptations. METHODS: We examined the functions of the BBSome (LpBBS1 and LpBBS2) in Lotmaria passim, a monoxenous trypanosomatid parasite infecting honey bees. The phenotypes resulting from depletion of LpBBS1 using the auxin-inducible degron system and disruption of LpBBS2 were characterized. RESULTS: Parasites deficient in LpBBS2 are smaller and less motile compared with wild-type. Although intraflagellar transport of a marker membrane protein is only mildly impaired, its association with lipid rafts is significantly disrupted in the mutants. This suggests that the BBSome is essential for maintaining lipid raft integrity in L. passim. Transcriptomic comparisons between wild-type and LpBBS2-deficient parasites reveal that the BBSome may also influence processes related to metabolism, membrane localization of specific proteins, DNA repair, microtubules, and mitochondria. CONCLUSIONS: In contrast to Leishmania mexicana, the BBSome in L. passim is crucial for efficient infection of the honey bee gut, demonstrating that its cellular functions vary between related trypanosomatid species. The BBSome is likely an adaptor that links multiple proteins in a species-specific manner under various cellular contexts.