The mechanistic Target of Rapamycin Complex 1 (mTORC1) couples nutrient sufficiency to cell growth, and is an important therapeutic target, notably in cancers. Amino acids can be up-taken in free form from transporters, and detected by different protein complexes that control the nucleotide-binding status of small GTPases of the Rag families. Nucleotide-bound Rag proteins recruit mTORC1 to the surface of the lysosome to mediate its full activation. A less well-characterized pathway of amino acid uptake is through macropinocytosis, in which extracellular proteins are endocytosed and delivered to the lysosome where they are degraded to amino acids, which also results in mTORC1 activation. Macropinocytosis is importantly enhanced by oncogenic KRAS mutations, and is thought to contribute to cancer survival in conditions of low free nutrient supply. Leveraging a proximity-dependent map of a human cell (Go, Knight et al., in prep), we generated proximity-dependent biotinylation “sensors” to study the recruitment of mTORC1 components to the surface of the endolysosomes. This revealed an unsuspected role for the HOPS trafficking complex in the activation of mTORC1 specifically in macropinocytic contexts. We also defined different roles for HOPS and the previously characterized GATOR2 complex in the mechanisms of mTORC1 activation downstream of specific nutrient acquisition pathways. Together, our results help understanding the mechanisms of growth regulation by macropinocytosis, and may offer new therapeutic avenues for cancers in which this pathway is upregulated.