Maintaining and monitoring genetic variation in natural populations is of crucial importance for conservation and management. Reductions in genetic diversity may have short term consequences in terms of increased inbreeding depression as well as long term effects by reducing the evolutionary potential of the population and decreasing the resilience against environmental change. With the developments in high throughput sequencing and genotyping it has now become possible to identify and monitor adaptive and neutral genetic variation at a genome-wide scale. Scandinavian wolverine (Gulo gulo) populations are subjected to habitat fragmentation and high mortality from poaching due to conflicts with livestock herders. Genetic monitoring is already an important part of the conservation programmes for this population, but the resolution and applications of genetic data have been hampered by a lack of genomic tools. Our wolverine genome assembly and re-sequencing analyses revealed a genetic diversity among the lowest ever detected in a red-listed population. Demographic analyses indicate that there has been a long-term decline of the effective population size, starting well before the last glaciation. We also found strong genome-wide signatures of inbreeding, but this effect was not observed when analysing a set of highly variable SNP markers for extended genotyping, illustrating that such markers can give a biased picture of the overall character of genetic diversity. Population genomic analyses revealed significant population structure with implications for connectivity and conservation. We used an integrated microfluidic circuit chip technology to develop an SNP-array consisting of 96 highly informative markers that, together with a multiplex pre-amplification step, was successfully applied to low-quality DNA from non-invasively collected scat samples. This work will facilitate management, conservation actions and genetic monitoring of wolverines, and also serves as a genomic roadmap that can be applied to conservation monitoring of other endangered species.