Background It is often assumed that local sexual networks play a dominant role in HIV spread in sub-Saharan Africa. However, the extent to which continued HIV transmission in rural African communities, home to two-thirds of the continent’s population, is driven by intra-community sexual networks versus viral introductions from outside of communities remains unknown.

Methods We analysed the spatial dynamics of HIV transmission in rural Rakai District, Uganda using population-based cohort data on 14594 individuals within 46 communities experiencing a generalised HIV epidemic (prevalence 12·%, incidence ∼2 per 100 person years). We applied spatial clustering statistics, phylogenetic analyses, and probabilistic transmission models to quantify the relative contributions of viral introductions versus local HIV transmission, including household transmission, to HIV incidence.

Results Individuals in households with incident (n = 189) or prevalent (n = 1597) HIV-infected persons were 3·2 (95% CI: 2·7–3·7) times more likely to be HIV-infected, compared to the population in general, but spatial clustering outside of households was weak and confined to distances < 500m. There was high viral diversity: only 34% of infected persons phylogenetically clustered with at least one other participant. One-third of phylogenetic clusters were individuals sharing a household. Of the remaining two-thirds, 71% crossed community boundaries. We estimate that 39% (95% CI: 32–44%) of viral transmissions occurred within stable household partnerships and that 40% (95% CI: 34–42%) of transmissions were from named extra-household sexual contacts, of which 62% (95% CI: 55–70%) were non-stable partners from outside the community.

Interpretation: External HIV introductions into rural communities are common and account for a substantial proportion of new HIV infections in Rakai, Uganda. Our findings suggest that combination HIV prevention will most effectively control local HIV epidemics when implemented at broad spatial scales, and imply a need to identify key populations serving as sources of introduced infections into general populations.