Regulation of T cell signal strength by interleukin 2 inducible T cell kinase (ITK) is a critical component in naïve CD4+ T helper (Th) and T regulatory (Treg) cell development. We hypothesized that absence of ITK activity will induce a switch in naïve T cell fate. Using ITK inhibitor CPI-818 (Corvus), we demonstrate that in the absence of ITK, naïve CD4+ T cells in Th17 conditions fail to generate pro-inflammatory Th17 cells and switch into generating Foxp3+ Treg-like cells. These switched Foxp3+ Treg-like cells resemble the anti-inflammatory Tregs in their suppressive function and global transcriptomic profile yet differ from both Th17 and Tregs in their chromatin landscape. We find that the mechanism involves calcium signaling because the switch response is prevented when intracellular calcium is enhanced by ionomycin treatment. This was associated with reduced expression of oxidative phosphorylation and glycolysis markers, reduced phosphorylation of mTOR-S6 signaling molecules and reduced expression of Th17 transcription factor BATF. We further investigated the effects of CPI-818 in vivo using the house dust mite induced model of allergic asthma, where CPI-818 treatment post development of lung inflammation significantly reduced the Th17 immune response. Taken together, we demonstrate that inhibition of ITK under Th17 differentiation conditions in vitro can induce the switch from pro-inflammatory Th17 to anti-inflammatory Treg cell fate via calcium signaling. This switch response is not limited to Th17 conditions, and ITK inhibition under conditions that promote anti-inflammatory T regulatory type 1 cell generation will also switch T cell fate to generating pro-inflammatory Th1-like cells. Altogether, this is significant because this potentially provides novel strategies to manipulate ITK and regulate balance of pro- and anti-inflammatory responses in health and disease.