In a world where habitats are degrading and the climate is warming and becoming increasingly unpredictable, biodiversity conservation efforts and funding remain grossly inadequate. There is a clear need to shift from preserving small, remnant populations to a model of genetically connecting populations that recreate larger and more diverse populations in climate-secure environments. This is crucial to harness key evolutionary processes to promote species’ ability to adapt to changing environments and to increase the likelihood of population persistence. Here, we use the endangered Macquarie perch (Macquaria australasica) as a case study to develop a genetic strategy for metapopulation management aimed at promoting population growth and persistence. Macquarie perch habitat has been highly fragmented and remaining habitat is at risk of catastrophic degradation due to climate change. We integrate results of new and existing genetic analyses to illustrate how genetically depauperate populations can benefit from admixture, and how the outcomes of management interventions can be quantified through genetic monitoring. We also develop the pipeline JeDi (https://github.com/drobledoruiz/JeDi) for estimating unbiased genetic heterozygosity for individuals and populations (nucleotide diversity) from reduced-representation genome sequencing data. We use this pipeline to estimate baseline data for monitoring of Macquarie perch populations and show that combining two genetic sources of migrants during population restoration resulted in doubling of nucleotide diversity compared to either source. Genetic diversity estimated using our pipeline is comparable across studies, datasets and species, and suitable for evaluating the rate of global biodiversity change.