How the nucleolus recovers from acute proteostatic stress, particularly in multinucleate syncytia, remains poorly understood. In the highly polarized hyphae of the model filamentous fungus Magnaporthe oryzae, we uncover a novel stress-induced spatial quality control pathway that promotes the inheritance of rejuvenated nucleolar material during nuclear division. This pathway discriminates between newly formed and damaged nucleolar compartments, selectively partitioning and sequestering the latter