The transmission of reliable information between individuals is crucial for group-living animals. This is particularly the case for cognitively advanced mammals with overlapping generations that acquire detailed social and ecological knowledge over long lifetimes. Here, we directly compare the ecological knowledge of elephants from two populations, with radically different developmental histories, to test whether profound social disruption affects their ability to assess predatory threat. Matriarchs (≤50 years of age) and their family groups received playbacks of three lions versus a single lion roaring. The family groups in the natural Amboseli population (Kenya) reliably assessed the greater predatory threat presented by three lions roaring versus one. However, in the socially disrupted Pilanesberg population (South Africa), no fine-scale distinctions were made between the numbers of roaring lions. Our results suggest that the removal of older and more experienced individuals in highly social species, such as elephants, is likely to impact the acquisition of ecological knowledge by younger group members, particularly through the lack of opportunity for social learning and cultural transmission of knowledge. This is likely to be exacerbated by the trauma experienced by juvenile elephants that witnessed the culling of family members and were translocated to new reserves. With increasing levels of anthropogenic disturbance, it is important that conservation practitioners consider the crucial role that population structure and knowledge transfer plays in the functioning and resilience of highly social and long-lived species.