Unlike most canids, versatile and capable of navigating vast landscapes, endangered Ethiopian wolves (Canis simensis) are endemic to an archipelago of Afroalpine islands. As a habitat specialist, the Ethiopian wolf is ill‐equipped to move across a highly transformed and densely populated agriculture matrix. Hard borders imposed by expanding subsistence agriculture lock Ethiopian wolves into further isolation, with few opportunities for dispersal and recolonisation. We report and evaluate empirical information from long‐term monitoring across the species' range to understand processes of habitat loss, recolonisation and extinction in recent and historical times, and to assess what conservation measures and strategies would ensure their persistence. Ethiopian wolves occurred in six isolated populations, totalling 454 wolves (population sizes ranged between 281 and 24) occupying 2700 km2 of Afroalpine habitat. We describe three population extinctions and three local extinctions within fragmented populations, and present evidence of factors accelerating the extinction process, such as disease (rabies and canine distemper virus), persecution, road kills and poisoning. Of all the suitable habitat available to wolves, 86% was included within nine protected areas, including three new Community Conservation Areas and two national park extensions in the past 10 years. As all Ethiopian wolf populations are small and vulnerable to stochastic events and environmental perturbation, conservation efforts to ensure the long‐term survival of the species need to integrate: 1) support for protected areas to halt agriculture encroachment and to regulate sustainable uses of natural resources; 2) efforts to minimise all causes of mortality, including but not limited to disease; and 3) conservation translocations to overcome fundamental barriers to dispersal in the highlands of Ethiopia.