<p>Immunotherapy has transformed cancer treatments, but the majority of cancer patients would inevitably develop resistance to immunotherapy. Th17 cells play complex but crucial roles in anti-cancer immune response, although their therapeutic potential remains underutilized. <i>Segmented filamentous bacteria</i> (<i>SFB</i>) function as prototypical commensal bacteria that can induce intestinal Th17 cells and impact host immune response. In this study, we investigated how <i>SFB</i> antigen-mediated immune responses modify the tumor microenvironment and enhance anti-tumor efficacy through a coordinated gut–lung immunological axis. We engineered B16F1 melanoma cells to express either the SFB3340 epitope (B16-3340, an I-A^b-restricted epitope derived from <i>SFBNYU_003340</i> and recognized by 7B8 TCR) or a control vector (B16-MEM) to evaluate <i>SFB</i> antigen effects on tumor immunogenicity. We found that expression of the <i>SFB</i> epitope in cancer cells decreased the number of lung tumor nodules, and <i>SFB</i> colonization further reduced tumor growth in a lung metastasis model. In addition, Th1, Th17, and CD8⁺ Tc1 cells were all increased in the lungs of the B16-3340 tumor-bearing mice compared with B16-MEM control tumor-bearing mice without triggering a compensatory expansion of immunosuppressive Tregs. Interestingly, <i>SFB</i> triggers systemic metabolic changes and an increase metabolites from aromatic amino acid degradation pathways, providing biochemical evidence for a functional gut–lung conduit, which integrates innate microbial detection with adaptive tumor-specific immunity. Our research provides evidence to further investigate and develop novel cancer immunotherapies that utilize microbial antigens and microbiome modifications to improve patient outcomes.</p>