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Anthropogenic activities have led to an unprecedented crisis in freshwater biodiversity loss. The capacity to monitor the abundance of wild populations is critical to conserving biodiversity, but conventional physical specimen collection methods are invasive, costly and labour-intensive. Environmental DNA (eDNA) offers a promising alternative, being easy to sample, with studies under controlled laboratory conditions showing consistent correlations between eDNA concentration and abundance. However, applying eDNA to monitor abundance remains contentious, as eDNA particle dynamics and the ecology of eDNA production can decouple this relationship in natural ecosystems. To address this, we provide a novel modelling method to produce population estimates from eDNA. We integrated bioenergetics and mass-balance frameworks to relate eDNA concentrations to freshwater fish population abundance estimated through conventional mark-recapture in Brook Trout (Salvelinus fontinalis) across nine Rocky Mountains lakes, five of which underwent size-selective harvesting over 2 years. Our integrated framework improved the variance explained in eDNA concentrations from 24% to 71%. The integrated model accurately distinguished most (94%) abundance estimates across populations and sampling periods, detecting both natural and harvest-induced reductions in abundance within several populations. This study is the first to empirically integrate the DNA production mechanism and particle dynamics and provide a new methodological approach enabling rapid and accurate abundance quantification. We also discuss how this new tool can be integrated in existing monitoring programmes.