The sodium leak channel (NALCN) conducts a neuronal background Na⁺ current that plays a crucial role in the regulation of breathing, sleep and movement. To perform these functions, NALCN has to associate with auxiliary subunits including UNC79, UNC80, and FAM155A. Functional disruptions of one of these evolutionarily conserved proteins have debilitating consequences ranging from apnoea, reversed circadian cycle to locomotor deficits. Despite its physiological significance, fundamental aspects regarding the organisation, composition and gating of the NALCN channelosome remain obscure, precluding a meaningful structure-function analysis. We determined the structure of this one megadalton complex, and discovered several unanticipated features. Contrary to previous speculations, the giant subunits UNC79 and UNC80 (2635 and 3258 amino acids, respectively) are highly structured, intertwined and anchored intracellularly to NALCN. We identified key regions in the interdomain linkers of NALCN that interact with UNC79 and UNC80, and showed that they are important for channel function using truncation and mutagenesis. Calmodulin (CaM), a previously uncharacterised component, copurifies with the channelosome. The intracellular activation gate of NALCN remains tightly shut even in the presence of all necessary components, incongruent with the expectation that a non-inactivating leak channel would have a constitutively open gate. However, single-channel recordings revealed an intrinsically low open-channel probability for NALCN, rationalising the non-conductive gate conformation captured. Together, these unprecedented glimpses into the architecture of the NALCN channelosome enabled us to decipher the contribution of individual component to function and to explore the gating mechanism of this machinery.