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Peanut (Arachis hypogaea L.) hairy roots are a potential tool for stilbene compound production. This study focuses on the most efficient elicitation strategy for inducing stilbene compound production, especially for the prenylated forms of trans-arachidin-1 and trans-arachidin-3. To the best of our knowledge, this is the first report of simultaneous treatment involving chitosan (CHT), methyl jasmonate (MeJA), and cyclodextrin (CD); CHT+MeJA+CD in peanut hairy roots to induce substantial amounts of trans-arachidin-1 and trans-arachidin-3 at 72 h of the elicitation period. The results demonstrate the highest amounts of trans-arachidin-1 and trans-arachidin-3, with 684.30 ± 183.85 and 543.94 ± 171.17 mg/g dry weight of hairy roots, respectively. The highest antioxidant capacity determined by ABTS and FRAP assays was 188.95 ± 0.43 µmol Trolox/g dry weight of hairy roots and 24.61 ± 0.50 mg ascorbic acid/g dry weight of hairy roots, respectively, while the highest phenolic content was also detected in this crude extract, with 8.67 ± 0.11 mg gallic acid/g dry weight of hairy roots. The antioxidant and pro-oxidant activity of the CHT+MeJA+CD crude extract in the protection and damage of DNA is of great interest and can have major positive impacts on health promotion and disease prevention.