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Peri-urban lakes increasingly experience intensified anthropogenic impacts as watershed uses and developments increase. Cultus Lake is an oligo-mesotrophic, peri-urban lake near Vancouver, British Columbia, Canada that experiences significant seasonal tourism, anthropogenic nutrient loadings, and associated cultural eutrophication. Left unabated, these cumulative stresses threaten the critical habitat and persistence of two endemic species at risk (Coastrange Sculpin, Cultus population; Cultus Lake sockeye salmon) and diverse lake-derived ecosystem services. We constructed water and nutrient budgets for the Cultus Lake watershed to identify and quantify major sources and loadings of nitrogen (N) and phosphorus (P). A steady-state water quality model, calibrated against current loadings and limnological data, was used to reconstruct the historic lake trophic status and explore limnological changes in response to realistic development and mitigation scenarios. Significant local P loadings to Cultus Lake arise from septic leaching (19%) and migratory gull guano deposition (22%). Watershed runoff contributes the majority of total P (53%) and N (73%) loads to Cultus Lake, with substantial local N contributions arising from the agricultural Columbia Valley (41% of total N load). However, we estimate that up to 66% of N and 70% of P in watershed runoff is ultimately sourced via deposition from the nutrient-contaminated regional airshed, with direct atmospheric deposition on the lake surface contributing an additional 17% of N and 5% of P. Thus, atmospheric deposition is the largest single source of nutrient loading to Cultus Lake, cumulatively responsible for 63% and 42% of total N and P loadings, respectively. Modeled future loading scenarios suggest Cultus Lake could become mesotrophic within the next 25 years, highlighting a heightened need for near-term abatement of P loads. Although mitigating P loads from local watershed sources will slow the rate of eutrophication, management efforts targeting reductions in atmospheric-P within the regional airshed are necessary to halt or reverse lake eutrophication, and conserve both critical habitat for imperiled species at risk and lake-derived ecosystem services.