Dynein recruitment to the nuclear envelope is required for pre-mitotic nucleus-centrosome interactions in nonneuronal cells and for apical nuclear migration in neural stem cells. In each case, dynein is recruited to the nuclear envelope (NE) specifically during G2 via two nuclear pore-mediated mechanisms involving RanBP2-BicD2 and Nup133-CENP-F. The mechanisms responsible for cell-cycle control of this behavior are unknown. We now find that Cdk1 serves as a direct master controller for NE dynein recruitment in neural stem cells and HeLa cells. Cdk1 phosphorylates conserved sites within RanBP2 and activates BicD2 binding and early dynein recruitment. Late recruitment is triggered by a Cdk1-induced export of CENP-F from the nucleus. Forced NE targeting of BicD2 overrides Cdk1 inhibition, fully rescuing dynein recruitment and nuclear migration in neural stem cells. These results reveal how NE dynein recruitment is cell-cycle regulated and identify the trigger mechanism for apical nuclear migration in the brain. Display omitted •Cdk1 triggers G2 nuclear envelope dynein recruitment for apical nuclear migration•Cdk1-phosphorylated RanBP2 binds BicD2 for early nuclear envelope dynein recruitment•Cdk1 induces nuclear export of CENP-F for late nuclear envelope dynein recruitment•Forced BicD2 recruitment to the nuclear envelope rescues Cdk1 inhibition Neural stem cells undergo motor protein-dependent nuclear oscillations between mitotic divisions, but how nuclear migration regulation is linked to the cell cycle has been unclear. Baffet et al. report that Cdk1 activates dynein recruitment to the nuclear pores during G2 phase through an effect on the dynein recruitment factors BicD2 and CENP-F.