Myriad abiotic stress responses in plants are controlled by abscisic acid (ABA) signaling, and ABA receptor proteins are recently studied to be degraded by the 26S proteasome pathway and by vacuolar degradation after processing via endosomal sorting complex required for transport (ESCRT) proteins. Despite their known essentiality in ABA signaling, the upstream regulators of ESCRTs remain unknown. Here, we report that the ESCRT-I component VPS23A is an unstable protein that is degraded via the ubiquitin-proteasome system. The UEV domain of VPS23A physically interacts with the two PSAP motifs of XBAT35, and this interaction results in the deposition of K48 polyubiquitin chains on VPS23A, thusly targeting it for degradation via 26S proteasomes. We show that XBAT35 in plants is a positive regulator of responses to ABA that acts via the VPS23A/PYL4 complex, specifically by accelerating VPS23A turnover, thereby increasing accumulation of the ABA receptor PYL4. Thus, beyond offering the first demonstration of how an ESCRT component is regulated in plants, this study deepens our understanding of plant stress responses by illustrating a mechanism wherein crosstalk between the ubiquitin-proteasome system (UPS) and endosome-vacuole mediated degradation pathways controls ABA signaling.