We currently have little idea where Mycobacterium tuberculosis (Mtb) transmission occurs in high incidence settings. Molecular studies suggest that only around 8-19% of transmission to adults occurs within-household, or between known social-contacts. This contrasts with findings from social-contact studies, which show that substantial proportions of contact time occur in households, workplaces and schools. A mathematical model of social-contact behaviour and Mtb transmission was developed, incorporating variation in susceptibility and infectiousness. Three types of contact were simulated: household, repeated (individuals outside household contacted repeatedly with daily-monthly frequency) and non-repeated. The model was parameterised using data from Cape Town, South Africa, on mean and variance in contact numbers and contact durations, by contact type, and fitted to an estimate of overdispersion in numbers of secondary cases ('superspreading') in Cape Town. Household, repeated, and non-repeated contacts contributed 36%, 13%, and 51% of contact time, and 13%, 8%, and 79% of disease, respectively. Results suggest contact saturation, exacerbated by long disease durations and superspreading, cause the high proportion of transmission between non-repeated contacts. Household and social-contact tracing is therefore unlikely to reach most tuberculosis cases. A better understanding of transmission locations, and methods to identify superspreaders, are urgently required to improve tuberculosis prevention strategies.