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The long-term functioning of metazoan tissues relies on the constant renewing of their cells. This renewing occurs by the production of new cellular material by various populations of proliferating cells. Sponges are well-known for the plasticity and high renewing rates of their tissues. Using immunocytochemistry, confocal microscopy, flow cytometry, bulk RNA sequencing, and experimental approaches we have extensively characterized cell proliferation in intact tissues and during various regeneration processes in cold-water calcareous sponge Leucosolenia corallorrhiza and demosponge Halisarca dujardinii. Intact tissues of both species contain broad populations of roliferating cells, most of which are choanocytes. Proliferating choanocytes have relatively slow cell cycles: 40 h in H. dujardinii and 60 h in L. corallorrhiza. EdU pulse-chase experiments show that in H. dujardinii, choanocyte progeny contributes to the renewing of other cell populations, while L. corallorrhiza seems to have rather independent proliferating populations in choanoderm and exopinacoderm. Both species retain active proliferation during regeneration processes, however, it seems dispensable to the replacement of the lost tissues: its inhibition with aphidicolin does not prevent or slow the restoration. Concordantly, RNA-seq data demonstrate the general downregulation of cell cycle genes during the whole regeneration process. Overall, our data support the notion of high renewing rates of sponge tissues relying on the actively proliferating choanocyte population. In contrast, various regeneration processes in sponges seem to be proliferative-independent and morphallactic in their nature.