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Beetroot has been traditionally used in folk medicine to treat various gastrointestinal disorders and is commonly consumed for its high antioxidant content. The primary objective of this study is to demonstrate, for the first time, the potential therapeutic effects of beetroot juice (BJ) in a rat model suffering from ulcerative colitis (UC) induced by dextran sulfate sodium (DSS). In addition, the study aims to identify the bioactive compounds in beetroot responsible for these effects. UC was induced in rats through the oral administration of DSS dissolved in drinking water (5%) during the final week of a 21-day treatment with BJ (5 and 10 mL/kg body weight) and compared to a reference drug, mesalazine. Phytochemical analysis revealed that BJ is a rich source of secondary metabolites such as polyphenols, flavonoids, soluble sugars, and betalains. The pretreatment with BJ significantly and dose-dependently reduced DSS-induced colonic mucosa lesions and associated histopathological alterations. The protective effects of BJ on the colonic mucosa were closely linked to its ability to mitigate oxidative damage, inflammatory injury, and biochemical imbalances. Specifically, BJ counteracted DSS-induced lipid peroxidation and restored levels of both enzymatic and nonenzymatic antioxidants. Moreover, BJ significantly decreased the levels of inflammatory markers and cytokines in plasma and colonic mucosa, while enhancing plasma scavenging activity and maintaining the homeostasis of intracellular mediators such as hydrogen peroxide, free iron, and ionizable calcium. These findings supported the use of BJ as a complementary approach for managing UC and underscore the need for further investigation into its potential clinical applications.