Major endogenous biochemical properties can make plants ideal agents for metal/metalloid-contaminated site cleanup. This study investigates the biochemistry of Juncus maritimus (Lam) roots for its high mercury (Hg) stabilization potential in the sediments of the Ria de Aveiro coastal lagoon (Portugal), which received Hg-rich effluents from a chlor-alkali industry between 1950 and 1994. J. maritimus plants were collected at a reference (R) site and three sites with the highest (L1), moderate (L2), and the lowest (L3) Hg contamination levels. The highest Hg-harboring/stabilizing J. maritimus roots at L1, exhibited significantly elevated damage endpoints (H2O2; lipid peroxidation, LPO; electrolyte leakage, EL; protein oxidation, PO; proline) which were accompanied by differential changes in H2O2-metabolizing defense system components (ascorbate peroxidase, catalase, glutathione peroxidase, glutathione S-transferase), glutathione reductase and the contents of both reduced and oxidized glutathione. Trends in measured endpoints reached maximum levels at L1 followed by L2 and L3. Cross-talks on root-Hg status and the studied biochemical traits revealed (a) high Hg-accrued elevations in oxidative stress as an obvious response; (b) Hg-stabilization potential of J. maritimus roots as a result of a successful mitigation of elevated high Hg-induced H2O2, and its anomalies such as LPO, EL, and PO; and (c) the induction of and a fine synchronization between non-glutathione and glutathione-based systems. Overall, the study unveiled biochemical mechanisms underlying root tolerance to Hg burden-accrued anomalies which, in turn, helped J. maritimus during Hg-stabilization.