The transcriptional regulator Rbpj is involved in T-helper (T) subset polarization, but its function in T cells remains unclear. Here we show that T-specific Rbpj deletion leads to splenomegaly and lymphadenopathy despite increased numbers of T cells with a polyclonal TCR repertoire. A specific defect of Rbpj-deficient T cells in controlling T2 polarization and B cell responses is observed, leading to the spontaneous formation of germinal centers and a T2-associated immunoglobulin class switch. The observed phenotype is environment-dependent and can be induced by infection with parasitic nematodes. Rbpj-deficient T cells adopt open chromatin landscapes and gene expression profiles reminiscent of tissue-derived T2-polarized T cells, with a prevailing signature of the transcription factor Gata-3. Taken together, our study suggests that T cells require Rbpj to specifically restrain T2 responses, including their own excessive T2-like differentiation potential.