To understand the mechanisms underlying the cell cycle regulation of vesicle-mediated membrane addition to the cytokinesis furrow, this study follows the localization and regulation of Nuf, a Rab11 effector, in the early Drosophila embryo. Nuf, and its mammalian homolog FIP3, is required for activating recycling endosome-based membrane delivery to the cytokinesis furrow. We used molecular genetic, biochemical, cell biological, and fluorescent confocal imaging techniques to determine that Nuf/FIP3 is a phosphoprotein whose pericentrosomal localization is regulated throughout the cell cycle. We show that Polo kinase directly phosphorylates two residues of Nuf, Ser225 and Thr227, and that phosphorylation of these sites correlates with Nuf being driven off the centrosome and into the cytoplasm during prophase, after furrow formation is complete. Further, reduced polo expression results in prolonged maintenance of Nuf at the centrosome. Conversely, increased polo expression limits Nuf association at the centrosome during interphase.