Significance The coreceptors of phytohormone ABA, such as ABI1, are the central regulator of plant tolerance to drought and other abiotic stresses. Tight regulation of ABI1 through ubiquitination is vital for ABA signaling and drought tolerance. In this study, we identified a mechanism to reduce ABI1 protein levels by an E2-E3 pair UBC27–AIRP3. UBC27 directly binds ABI1 and cooperates with AIRP3 in the degradation of ABI1 and ABA signaling. ABA further activates the expression of UBC27 and AIRP3 , inhibits the degradation of UBC27, and enhances the interaction between UBC27 and ABI1, establishing a positive feedback regulatory loop to control UBC27 activity under stress conditions. Our results identify a layer of ABA-pathway regulation that terminates ABI1 by the ubiquitination complex UBC27–AIRP3.