Mechanistic target of rapamycin complex 1 (mTORC1) coordinates cellular growth with nutrient availability through signalling at the lysosomal membrane. Central to this pathway, the KICSTOR-GATOR1 complex suppresses mTORC1 during amino acid starvation by stimulating Rag GTPase hydrolysis, yet the molecular basis of KICSTOR-mediated regulation has remained unknown. Here, we combine cryo-electron microscopy, biochemical reconstitution, quantitative cell signalling assays, and live-cell imaging to define the architecture and mechanism of this essential nutrient-sensing assembly. We resolve the complete seven-subunit KICSTOR-GATOR1 complex, revealing an elongated crescent-shaped scaffold in which the 3,432-residue SZT2 subunit recruits GATOR1 through an extensive interface with NPRL3. Structure-guided mutagenesis demonstrates that this interface is essential for lysosomal mTORC1 inhibition during amino acid starvation. We further determine the structure of the methionine sensor SAMTOR bound to KICSTOR, showing that SAMTOR engages SZT2 in a conformation that is incompatible with S-adenosylmethionine binding, providing a structural explanation for methionine-dependent control of mTORC1. Finally, we identify a higher-order KICSTOR-GATOR1 supercomplex assembled through DEPDC5-mediated GATOR1 dimerisation. This arrangement favours the GAP-active mode of Rag engagement while sterically restricting the inhibitory binding mode, revealing a previously unrecognised mechanism that promotes RagA GTP hydrolysis. Together, these findings establish the structural framework for lysosomal nutrient sensing and explain how KICSTOR spatially organises GATOR1 to regulate mTORC1 signalling.