Phosphate (Pi) is essential for plant growth and is acquired by the plasma membrane (PM) PHOSPHATE TRANSPORTER 1 proteins (PHT1s). Enhancing the abundance of PHT1s at the cell surface under Pi limitation thus ensures plant productivity. CORNICHON HOMOLOG proteins (CNIHs) are eukaryotic conserved cargo receptors that selectively mediate the endoplasmic reticulum (ER) export of membrane proteins. We identified theArabidopsis thaliana CNIH5(AtCNIH5) as a Pi starvation-inducibleCNIHgene preferentially expressed in the outer root cell layers above the meristem.AtCNIH5 localizes adjacent to theAtSEC16A-labeled ER exit sites and interacts withAtPHT1;1 and PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 (AtPHF1). Loss ofAtCNIH5confers reduced shoot Pi levels and decreasedAtPHT1s but increasedAtPHF1. The root hair and the epidermis within the transition/elongation zone of thecnih5mutant display a lower PM targeting efficiency ofAtPHT1;1. Moreover, dysfunctionalAtCNIH5 exerts a suppressive effect on the growth ofphf1and alleviates Pi toxicity in the Pi overaccumulatorpho2. However, thein vivoprotein–protein interaction and degradation assays indicated thatAtCNIH5 is unlikely a direct target ofAtPHO2. Our findings highlight that low Pi-responsiveAtCNIH5 interplays withAtPHF1 to promote the PM targeting ofAtPHT1s in a cell type-dependent manner.Synopsis:Phosphate starvation-induced CNIH5 acts as an ER cargo receptor of PHT1 transporters inArabidopsis, enhancing their plasma membrane targeting and phosphate uptake.The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell/pages/General-Instructions) is: Tzu-Yin Liu (tzliu@life.nthu.edu.tw).