The nuclear pore complex (NPC) is a cornerstone of eukaryotic cell functionality, orchestrating the nucleocytoplasmic shuttling of macromolecules. Here we report that Plant Nuclear Envelope Transmembrane 1 (PNET1), a transmembrane nucleoporin, is an adaptable NPC component that is mainly expressed in actively dividing cells. PNET1's selective incorporation into the NPC is required for rapid cell growth in highly proliferative meristem and callus tissues in Arabidopsis. We demonstrate that the cell cycle-dependent phosphorylation of PNET1 coordinates mitotic disassembly and post-mitotic reassembly of NPCs during the cell cycle. PNET1 hyperphosphorylation disrupts its interaction with the NPC scaffold, facilitating NPC dismantling and nuclear membrane breakdown to trigger mitosis. In contrast, nascent, unphosphorylated PNET1 is incorporated into the nuclear pore membrane in the daughter cells, where it restores interactions with scaffolding nucleoporins for NPC reassembly. The expression of the human PNET1 homologue is required for and markedly upregulated during cancer cell growth, suggesting that PNET1 plays a conserved role in facilitating rapid cell division during open mitosis in highly proliferative tissues.