It has long been recognized that superior carnivores can impact on the demography and ecology of smaller members of the guild, although exact mechanisms remain unclear. Here we use original data from a unique natural experiment to study some of the mechanisms by which African lions Panthera leo impact on African wild dogs Lycaon pictus. Using a study site where wild dogs outnumbered lions for several years prior to lion population recovery, we aimed to investigate whether or not, and by which means, wild dog populations are regulated and influenced by lions. We used 38 pack‐years of demographic and behavioural data across two 4‐year periods where lion density differed 20‐fold (pre‐lion era: 1996–1999 and lion era: 2010–2013) to assess how lions may affect wild dog pack size and age structure, litter size and pup survival (n = 329 pups), as well as den site selection (n = 46 dens). Pack size was significantly greater during the pre‐lion era. The pup to adult ratio was lower during the lion era and the change in pack composition was directly attributable to significantly greater lion‐induced pup mortality. We also demonstrate a behavioural shift, with locations selected for the vulnerable denning period being in more rugged terrain and in areas with lower prey densities during the lion era, as compared with the pre‐lion era. Lower adult recruitment into a population of an obligate cooperative breeder like the African wild dog can have complex consequences, including on feeding and defence of young, and mate finding.