The lysosome is a cellular organelle often referred to as the “trashcan” of the cell due to its primary function to digest and recycle unneeded or damaged intracellular material. The endoplasmic reticulum (ER) is a vast intracellular network of membranes, which function as the manufacturing center for macromolecules of the cell. The lysosome and ER carry out critical, yet seemingly opposing, functions of catabolism and anabolism, thus it is essential that the organelles be in constant communication to ensure cellular homeostasis. However, a method of communication between the lysosome and ER has yet to be identified. In this study, we performed a genetic screen to understand what functional regulators of the lysosome impact ER homeostasis. Through these screens, we found a lysosomal amino acid transporter, LAAT-1. Specifically, LAAT-1 is involved in export of recycled lysine and arginine from the lysosome, and this process is critical for proper function of ER quality control machineries. Without LAAT-1, the ER is highly susceptible to damage. Mutations in LAAT-1 increase stress sensitivity and decrease organismal health and lifespan. Ultimately, our studies show that lysosomal recycling of key amino acids are critical for regulating ER function, which has direct implications in organismal physiology and lifespan.