Lysosomes play crucial roles in regulating eukaryotic metabolism and cell growth by acting as signalling platforms to sense and respond to changes in nutrient and energy availability. LYCHOS (GPR155) is a lysosomal transmembrane protein that functions as a cholesterol sensor, facilitating the cholesteroldependent activation of the master protein kinase mechanistic target of rapamycin complex 1 (mTORC1). However, the structural basis of LYCHOS assembly and activity remains unclear. Here, we determine several high-resolution cryo-electron microscopy (cryo-EM) structures of human LYCHOS, revealing a homodimeric transmembrane assembly of a transporter-like domain fused to a G proteincoupled receptor (GPCR) domain. The class B2-like GPCR domain is captured in the apo state and packs against the surface of the transporter-like domain, providing a highly unusual example of a GPCR as a domain in a larger transmembrane assembly. Cholesterol sensing is mediated by a conserved cholesterol-binding motif, positioned between the GPCR and transporter domains. We reveal that the LYCHOS transporter-like domain is an orthologue of the plant PIN FORMED (PIN) auxin transporter family with greater structural similarity to plant auxin transporters than known human transporters. Activity assays support a model whereby the LYCHOS transporter and GPCR domains coordinate to sense cholesterol and regulate mTORC1 activation.