Stimulator of Interferon Genes (STING), a critical player in cytosolic DNA sensing, has been shown to be required for anti-tumor responses, illustrating the potential of STING-targeting for cancer immunotherapy. The cyclic dinucleotide Cyclic guanosine monophosphate–adenosine monophosphate (2’3’-cGAMP) is a STING agonist which induces TBK1/IRF3-dependent production of Type I IFN and leads to potent antitumor properties in mouse models of cancers by triggering innate immune response. While recent studies evidenced that STING ligands can activate STING signaling in T cells, their effects on CD4 T cell differentiation and anti-tumor functions remain to be determined. Here, we show that the transfection of 2’3’-cGAMP enhances IL-9 and IFN-γ secretion from differentiating Th9 and Th1 effector cells, respectivelly, in a STING-dependent manner. We found that P65 NF-KB appears involved in both 2’3’-cGAMP-driven production of IFN-γ and IL-9 while IRF3 is only required for 2’3’-cGAMP-driven production of IFN-γ. Because Th1 and Th9 cells exert antitumor functions, we investigated their involvement in the antitumor activity of 2’3’-cGAMP in vivo. Treatment of tumor-bearing mice with antibodies neutralizing IFN-γ and IL-9 strongly impairs the capacity of 2’3’-cGAMP to reduce tumor growth. We also demonstrate that 2’3’-cGAMP treatment enhances Th9 anticancer functions when adoptively transferred into mice. Overall, this study uncovers a novel cell-intrinsic role for STING in modulating CD4 T cell differentiation and shaping adaptive antitumor immune responses. The contribution of CD4 T cells in 2’3’-cGAMP antitumor activity brings important insights for the design of immunotherapies involving STING activation.