Metabolic dysfunction–associated steatohepatitis (MASH)-associated liver fibrosis remains without effective therapeutic options, and the contribution of gut microbiota-derived metabolites to fibrotic progression is incompletely understood. In this project, we identified a microbiota–metabolite–host signaling axis involving dietary flavonoids, Streptococcus salivarius, and 3,4-dihydroxyphenylacetic acid (DHPAA). Rifaximin treatment reshaped the gut microbiota and enriched S. salivarius, which exhibited anti-fibrotic effects and improved intestinal barrier integrity. Metabolomic analyses revealed that DHPAA was increased in feces, portal circulation, and liver tissues, and supplementation with DHPAA reproduced the protective effects of S. salivarius by reducing hepatic stellate cell activation and collagen deposition. Mechanistically, DHPAA activated the aryl hydrocarbon receptor (AHR) pathway and suppressed INHBB, TGF-β, and Notch signaling. Dietary flavonoids enhanced DHPAA production and alleviated fibrosis across multiple experimental models. These findings identify a microbiota–metabolite–host signaling axis and highlight S. salivarius-derived DHPAA as a potential therapeutic target for MASH-associated liver fibrosis.