Anthropogenic pressures can have detrimental impacts on fish populations, with their effective management and conservation requiring accurate monitoring tools. Yet, this is not straightforward for closely-related, co-existing species that are difficult to distinguish using simple phenotypic or genetic approaches. Coregonids are of cultural and economic importance across Europe but have faced a multitude of pressures over the last century. Yet genomic management tools are lacking. In Lake Constance, a large pre-alpine lake, stocks have drastically collapsed due to a multitude of pressures, leading to a fishery closure. Here, we adopt a cost-effective, whole genome sequencing approach for lake-wide assessment of stock composition, spatial distribution and genetic diversity of highly admixed Lake Constance whitefish (Coregonus spp.). By sequencing 983 adult and larval genomes, we show that nearly 90% of the stock is made up by one of three species, the Gangfisch (C. macrophthalmus), and define the genetic relationship between Upper and Lower Lake Constance whitefish stocks. We also identified strong mixing between Gangfisch and Blaufelchen (C. wartmanni) on traditionally specific-specific spawning grounds, and detected strong admixture in larvae, with potentially drastic impacts on the effectiveness of hatchery supplementation and stocking. Despite the collapse and admixture, species still exhibit low to moderate levels of genetic diversity, maintain ecologically-relevant genetic differences, and seem to show differences in habitat use. Overall, we present a cost-effective, translatable tool for stock-wide sequencing and genetically-informed fisheries management, with our results calling for the re-evaluation of current management practices to avoid the potential genetic m