Small, isolated populations are at greater risk of genome erosion than larger populations. Successful conservation efforts may lead to demographic recovery and mitigate the negative genetic effects of bottlenecks. However, life-history traits and mating behaviour can hamper genomic recovery. Here, we use population genomic analyses and forward simulations to assess the genomic impacts of near extinction in the isolated Ngorongoro Crater lion (Panthera leo) population. We show that 200 years of isolation and the recent epizootic in 1962 resulted in a two-fold increase in inbreeding and an excess in the frequency of highly deleterious mutations relative to the Greater Serengeti population. However, there was little evidence for purging of genetic load through a gradual increase in inbreeding. Furthermore, forward simulations indicate that low gene flow from outside of the Crater may contribute to future genome erosion in the population, with a minimum of one to five effective male migrants per decade required to reduce the risk of long-term inbreeding depression and reduction in genetic diversity. Our results suggest that in spite of a rapid post-epizootic demographic recovery since the 1970s, strong male territoriality may contribute to the genetic isolation of the population, further exacerbating the effects of genome erosion.