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Withaferin A (WFA) is a bioactive constituent derived from the <jats:italic>Withania somnifera<\/jats:italic> plant, which has extensive pharmacological activities; however, little is known about the regulatory role of SIRT3 in the WFA-induced antifibrogenic effect. The current study is aimed at investigating the role of SIRT3 in WFA-induced antioxidant effects in liver fibrosis. Our study verified that WFA attenuated platelet-derived growth factor BB- (PDGF-BB-) induced liver fibrosis and promoted PDGF-BB-induced SIRT3 activity and expression in JS1 cells. SIRT3 silencing attenuated the antifibrogenic and antioxidant effects of WFA in activated JS1 cells. Moreover, WFA inhibited carbon tetrachloride- (CCl<jats:sub>4<\/jats:sub>-) induced liver injury, collagen deposition, and fibrosis; increased the SIRT3 expression; and suppressed the CCl<jats:sub>4<\/jats:sub>-induced oxidative stress in fibrotic livers of C57\/BL6 mice. Furthermore, the antifibrogenic and antioxidant effects of WFA could be available in CCl<jats:sub>4<\/jats:sub>-induced WT (129S1\/SvImJ) mice but were unavailable in CCl<jats:sub>4<\/jats:sub>-induced SIRT3 knockout (KO) mice. Our study suggested that WFA inhibited liver fibrosis through the inhibition of oxidative stress in a SIRT3-dependent manner. 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