The Rag GTPases act as a molecular switch that controls mTORC1 activation at the lysosome in response to amino acid availability. Under nutrient-poor conditions, the GATOR1 complex functions as a GTPase-activating protein (GAP) for RagA, suppressing mTORC1 signalling. KICSTOR is required to recruit and regulate GATOR1 at the lysosome, but the molecular basis of this interaction has remained unclear. Here, we determine the structure of the KICSTOR–GATOR1 assembly, revealing a striking ~60 nm crescent-shaped architecture. We show that GATOR1 engages KICSTOR through an extensive interface essential for lysosomal localization and mTORC1 regulation. Unexpectedly, KICSTOR and GATOR1 assemble into a larger dimeric supercomplex, generating a higher-order docking platform at the lysosome. This dimeric organisation constrains the orientation of GATOR1, favouring a low-affinity, catalytically active mode of Rag GTPase engagement while sterically occluding the high-affinity inhibitory configuration. Together, these findings define the structural basis of GATOR1 regulation by KICSTOR and establish dimerization as a key principle governing nutrient-dependent mTORC1 control at the lysosome.