Historical mining left a legacy of abandoned mines and waste rock in remote headwaters of major river systems in the western United States. Understanding the influence of these legacy mines on culturally and ecologically important downstream ecosystems is not always straightforward because of elevated natural levels of mineralization in mining‐impacted watersheds. To test the ecological effects of historic mining in the headwaters of the upper Salmon River watershed in Idaho (USA), we measured multiple community and chemical endpoints in downstream linked aquatic–terrestrial food webs. Mining inputs impacted downstream food webs through increased mercury accumulation and decreased insect biodiversity. Total mercury (THg) in seston, aquatic insect larvae, adult aquatic insects, riparian spiders, and fish at sites up to 7.6 km downstream of mining was found at much higher concentrations (1.3–11.3‐fold) and was isotopically distinct compared with sites immediately upstream of mining inputs. Methylmercury concentrations in bull trout and riparian spiders were sufficiently high (732–918 and 347–1140 ng MeHg g−1 dry wt, respectively) to affect humans, birds, and piscivorous fish. Furthermore, the alpha‐diversity of benthic insects was locally depressed by 12%–20% within 4.3–5.7 km downstream from the mine. However, because total insect biomass was not affected by mine inputs, the mass of mercury in benthic insects at a site (i.e., ng Hg m−2) was extremely elevated downstream (10–1778‐fold) compared with directly upstream of mining inputs. Downstream adult aquatic insect–mediated fluxes of THg were also high (~16 ng THg m−2 day−1). Abandoned mines can have ecologically important effects on downstream communities, including reduced biodiversity and increased mercury flux to higher order consumers, including fish, birds, and humans. Environ Toxicol Chem 2022;41:1696–1710. Published 2022. This article is a U.S. Government work and is in the public domain in the USA.