The function of NF‐κB family members is controlled by multiple mechanisms including the transcriptional regulator Bcl‐3, an atypical member of the IκB family. By using a murine model of conditional Bcl‐3 overexpression specifically in T cells, we observed impairment in the development of Th2, Th1, and Th17 cells. High expression of Bcl‐3 promoted CD4+ T‐cell survival, but at the same time suppressed proliferation in response to TCR stimulation, resulting in reduced CD4+ T‐cell expansion. As a consequence, T‐cell‐specific overexpression of Bcl‐3 led to reduced inflammation in the small intestine of mice applied with anti‐CD3 in a model of gut inflammation. Moreover, impaired Th17‐cell development resulted in the resistance of Bcl‐3 overexpressing mice to EAE, a mouse model of multiple sclerosis. Thus, we concluded that fine‐tuning expression of Bcl‐3 is needed for proper CD4+ T‐cell development and is required to sustain Th17‐cell mediated pathology. Expression of Bcl‐3, an atypical member of NF‐κB inhibitors, is fine‐tuned in CD4+ T cells during development. Constitutive expression of Bcl‐3 prevents Th17‐cell development and results in resistance of mice to the induction of experimental autoimmune encephalomyelitis (EAE).