Bacterial cancer therapy (BCT) shows great promise for treatment of solid tumors, yet basic mechanisms of bacterial-induced tumor suppression remain undefined. The intestinal epithelium is the natural route of infection forSalmonellaand thus harbors innate immune defenses which protect against infection. Attenuated strains ofSalmonella entericaserovar Typhimurium (STm) have commonly been used in mouse models of BCT, largely with the use of xenograft and orthotopic transplant cancer models. We aimed to better understand the tumor epithelium-targeted mechanisms of BCT by using mouse models of intestinal tumorigenesis and tumor organoid cultures to assess the effectiveness and mechanisms of treatment with aromatase A-deficientSTm (STmΔaroA).STmΔaroAdelivered by oral gavage could significantly reduce tumor burden and tumor load in both a colitis-associated colon cancer model (CAC) and in a spontaneous intestinal cancer model,Apcmin/+mice.STmΔaroAcolonization of tumors caused alterations in transcription of mRNAs associated with epithelial–mesenchymal transition as well as metabolic and cell cycle-related transcripts. Metabolomic analysis of tumors demonstrated alteration in the metabolic environment ofSTmΔaroA-treated tumors, suggestingSTmΔaroAimposes metabolic competition on the tumor. Use of tumor organoid culturesin vitrodemonstrated thatSTmΔaroAcan directly affect the tumor epithelium with alterations in transcripts and metabolites similar toin vivo-treated tumors. Thereby, we demonstrate that bacterial cancer therapy is efficacious in autochthonous intestinal cancer models, that BCT imposes metabolic competition, and that BCT has direct effects on the tumor epithelium, which have not previously been appreciated.One Sentence SummaryAttenuatedSalmonella entericaserovar Typhimurium can home to gastrointestinal tumors and directly affect the tumor epithelium, inducing transcriptional and metabolic changes that lead to reduced tumor burden in mice.