Homoscleromorpha is a recently recognized class within the phylum Porifera. While molecular analyses support monophyly of Homoscleromorpha, morphological data are largely lacking. Here, we investigate and comparatively analyze the detailed morphology of kinetids (flagellar apparatus) in choanocytes of ten Oscarella species. The kinetid is known to be a phylogenetically important trait that can possibly reflect relationships of sponges at the level of orders. We also conduct a phylogenetic analysis based on previously published sequences. We found the family Oscarellidae is subdivided into two large groups, and choanocyte kinetids structure strongly supports this division. The first group includes Oscarella lobularis, O. tuberculata, O. bergenensis, O. viridis, O. rubra, O. malakhovi, O. microlobata, O. carmela, O. filipoi, and O. zoranja. These species possess nuclei located in a basal position without any connection to the kinetosome. The second group includes O. balibaloi, O. nicolae, O. kamchatkensis, O. pearsei, O. imperialis, and Pseudocorticium jarrei, whose nuclei are connected with the kinetosome. In addition, this second group also shares mesohylar spherulous cells harboring paracrystalline inclusions. The choanocyte kinetid structure seems to be an essential phylogenetic and diagnostic morphological trait, and we propose to include it in future species descriptions. Our results imply assignation of the second group to the genus Pseudocorticium. This taxonomic suggestion, however, needs additional data on the remaining Oscarella species.