Mercury bioavailability and biomagnification in freshwater systems can be highly variable; thus, tissue data from biosentinel taxa can be useful to assess risk. Dragonfly larvae have emerged as biological indicators of mercury impairment, yet their mercury biodynamics over time and across exposure levels are not well understood. Evaluating these attributes using controlled experimental approaches is an important step to validate larval dragonflies as biosentinels for spatial and temporal trends in mercury risk. We conducted an experimental series quantifying methylmercury trophic transfer from dosed prey to predatory dragonfly larvae at environmentally relevant concentrations. Dragonfly total mercury concentrations increased proportionally by factors of 2.7 to 4.2 with each doubling of prey methylmercury concentration, responding to dietary treatments in 7–28 days and reaching equilibrium in as little as 40 days, supporting their utility to indicate changing mercury exposure regimes. Dosed dragonflies biomagnified methylmercury by factors of 1.0 ± 0.1 to 3.4 ± 0.2 relative to their prey, and biomagnification efficiency decreased by over 40% for each doubling of prey methylmercury concentration. Dragonfly development had dose-dependent effects on bioaccumulation: mercury concentrations increased with growth and decreased with age in higher exposure treatments, whereas they decreased with growth and increased with age in lower exposure treatments. Bioaccumulation also varied taxonomically; within treatments, mean mercury concentrations for each genus varied up to 10% from family-level means. Dragonfly sex, size, and body condition did not significantly affect mercury concentrations. These results help validate and expand the utility of dragonfly larvae as biosentinels to monitor mercury risk and better protect wildlife and human health.