Adipose tissue is a key pharmacological target to prevent or treat the consequences of obesity. Adipose specific cell surface proteins are especially interesting due to their important roles in orchestrating cellular responses to environmental cues. Nutritionally-regulated adipose and cardiac enriched protein (Nrac) is a small adipocyte specific transmembrane protein with no known function. We show that Nrac modulates CD36 mediated fatty acid uptake, by forming a complex with CD36 and caveolin-1 under low extracellular fatty acid concentrations. Upon loss of Nrac or an increase in extracellular fatty acid levels, leading to reduced Nrac surface localization, CD36 dissociates from caveolin-1 and is internalized via clathrin mediated endocytosis. This results in increased fatty acid uptake into adipocytes, adipocyte hypertrophy, increased fat mass and elevated lipid clearance from the blood in chow diet fed mice. Thus, we unravel a novel regulatory mechanism of adipocyte fatty acid uptake dependent on its extracellular availability