Background: Hepatocellular carcinoma (HCC) is an aggressive malignancy with limited treatment options. The emerging field of tumor immunotherapy, primarily focusing on CD8⁺ T cells and the tumor microenvironment (TME), has garnered substantial attention. CD4⁺ T cells, on the other hand, play a crucial role in maintaining immune equilibrium and orchestrating immune responses through interactions with various cell types. As crucial participants and coordinators in innate and adaptive immune responses, the role of CD4⁺ T cells in tumor development remain further exploration. Conventional dendritic cells (cDCs) are thought to perform antigen presentation to prime CD4⁺ T cells or CD8⁺ T cells. However, the reverse regulatory impact of CD4⁺ T cells on cDCs remains poorly understood. Methods: Initially, we examined the role of CD4⁺ T cell subsets in HCC development using TCGA database. Subsequently, we established Cd4-Cre Bcl9^fl/flBcl9l^fl/fl mice to explore the impact of T cell-specific Bcl9/Bcl9l deficiency on HCC development. We further investigate the impact of Bcl9/Bcl9l deficiency in CD4⁺ T cells on the therapeutic efficacy of mouse CAR-T treatment. Moreover, using single-cell RNA sequencing (scRNA-seq) databases from Bcl9/Bcl9l KO tumor-bearing mice and HCC patients, we investigated the regulatory role of CD4⁺ T cells on the function of cDCs. Finally, we validated the mechanism by which CD4⁺ T cells regulate cDCs function in a mouse HCC model and explored their influence on tumor-specific CD8⁺ T cells response. Results: We found elevated Th1 cell infiltration in various cancers including liver hepatocellular carcinoma (LIHC). High Th1 infiltration is associated with a favorable prognosis in LIHC, but there is a significant negative correlation between the expression of B-cell lymphoma 9/B-cell lymphoma 9-like (BCL9/BCL9L) and the infiltration of Th1 cells. We found that blocking T cell-intrinsic BCL9/BCL9L increased frequencies of Th1 cells, thereby suppressing HCC tumor growth. The enrichment of Th1 cells inversely regulates innate immune response to augment cDCs activation. BCL9/BCL9L inhibition amplifies CD4⁺ T cell and cDCs crosstalk and promotes cDCs antigen presentation. The reinforced cross-presentation of tumor antigens by cDCs promotes activation and proliferation of CD8⁺ T cells. Moreover, genetic editing of BCL9/BCL9L in CD4⁺ T cells can enhance the anti-tumor immunity by promoting CAR-T cell toxicity. Conclusions: Thus, BCL9/BCL9L inhibition orchestrate an adaptive immune to innate immune circuit wherein Th1 cells triggers cDCs antigen presentation in turn activate tumor-specific CD8⁺ T cells response to promote cancer immunity.