Glucose-6-Phosphatase (G6Pase), a key enzyme in gluconeogenesis and glycogenolysis in the mammalian liver and kidney, converts glucose-6-phosphate to glucose to maintain systemic blood glucose homeostasis during nutrient deprivation. However, its function has remained elusive in insects which have no need for G6Pase in sugar homeostasis, since they use trehalose as the main circulating sugar and convert glucose-6-phosphate to trehalose via trehalose phosphate synthase (TPS1). This study reveals an unexpected and essential role for G6Pase in Drosophila fertility. We report that that Drosophila G6P mutant males are sterile and show that G6Pase plays an essential role to produce motile sperm. While spermatogenesis and spermiogenesis in G6P mutant males appears to proceed normally, leading to the production and transfer of mature sperm, G6P- sperm tail beat frequency is severely diminished in the female reproductive tract, and sperm only rarely enter an egg. Moreover, when compared to wild type sperm, G6P- sperm are depleted earlier from spermathecae and seminal receptacle. Immunohistochemical analyses show that G6P mutant spermatocytes present with an enlarged and stressed endoplasmic reticulum (ER) and a diminished Golgi. Additionally, the acrosome, a Golgi derived organelle critical for sperm-egg interaction, is partially depleted of the transmembrane protein SNEAKY, which is essential to breakdown the sperm plasma membrane after fertilization. Metabolic analyses show that both basal and compensatory glycolysis and ATP production are compromised in testes of G6P mutant males. Based on these observations, we propose a model in which Drosophila G6Pase functions as a metabolite repair enzyme in spermatocytes. By removing a non-canonical metabolite, G6Pase facilitates glycolysis to meet the high energy demands of spermatogenesis and sperm cell differentiation. Thus, our investigations unveil a novel function for G6Pase in male fertility, highlighting its importance in regulating energy homeostasis in reproductive tissues.