The dynamic maintenance of polar domains in the plasma membrane (PM) is critical for many fundamental processes, e.g., polar cell growth and growth guidance but remains poorly characterized. Rapid tip growth of Arabidopsis pollen tubes requires dynamic distribution of active ROP1 GTPase to the apical domain. Here, we show that clathrin-mediated endocytosis (CME) coordinates lateral REN4 with apical ROP1 signaling. REN4 interacted with but antagonized active ROP1. REN4 also interacts and co-localizes with CME components, but exhibits an opposite role to CME, which removes both REN4 and active ROP1 from the PM. Mathematical modeling shows that REN4 restrains the spatial distribution of active ROP1 and is important for the robustness of polarity control. Hence our results indicate that REN4 acts as a spatiotemporal rheostat by interacting with ROP1 to initiate their removal from the PM by CME, thereby coordinating a dynamic demarcation between apical and lateral domains during rapid tip growth.