AbstractCell wall synthesis and protein glycosylation require the import of nucleotide diphosphate–sugar conjugates into the Golgi that must be counterbalanced by phosphate (Pi) export. Numerous Golgi nucleotide-sugar transporters have been characterized, but transporters mediating Golgi Pi export remain poorly understood. We used plant and yeast genetics to characterize the role of 2 Arabidopsis (Arabidopsis thaliana) proteins possessing an EXS domain, namely ERD1A and ERD1B, in Golgi Pi homeostasis. ERD1A and ERD1B localized incis-Golgi and were broadly expressed in vegetative and reproductive tissues. We identified ERD1 putative orthologs in algae, bryophytes, and vascular plants. ExpressingERD1AandERD1Bin yeast complemented theerd1mutant phenotype of cellular Pi loss via exocytosis associated with reduced Golgi Pi export. The Arabidopsiserd1amutant had a similar phenotype of apoplastic Pi loss dependent on exocytosis.ERD1Aoverexpression inNicotiana benthamianaand Arabidopsis led to partial mislocalization of ERD1A to the plasma membrane and specific Pi export to the apoplastic space. Arabidopsiserd1ahad defects in cell wall biosynthesis, which were associated with reduced shoot development, hypocotyl growth, cell wall extensibility, root elongation, pollen germination, pollen tube elongation, and fertility. We identified ERD1 proteins as Golgi Pi exporters that are essential for optimal plant growth and fertility.