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This study evaluated the cytotoxic activity of two synthetic 1,4-naphthoquinones, compound 1 and its dual redox analog, compound 4, against NQO1-overexpressing DU-145 prostate cancer cells through integrated in vitro, enzymatic, and computational (docking and quantum) analyses. Compound 4 exhibited over 2-fold greater cytotoxicity against DU-145 cells compared to nontumor MRC-5 cells, while maintaining low hemolytic activity. Evidence of membrane damage, ROS generation, lipid peroxidation, and reversal by deferoxamine indicated ferroptosis induction by 4, whereas 1 triggered caspase-3-dependent apoptosis. Both caused ROS-mediated DNA damage attenuated by NAC. Docking and enzymatic assays confirmed partial dependence on NQO1, with 4 showing greater ROS production despite lower enzymatic activity. 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