Regulatory T (Treg) cells are essential for controlling inflammation and maintaining tissue homeostasis. Transcriptional intermediary factor 1-γ (TIF1γ) has been implicated in noncanonical TGFβ-Smad signaling in hematopoietic stem cells, but its role in Treg cell function has not been explored. Here we show that TIF1γ-deficient Treg cells lose Foxp3 expression and acquire effector phenotypes in a cell-intrinsic manner upon inflammatory challenge. In vivo, TIF1γ-deficient Treg cells adopt type 1 helper T cell-like or pro-inflammatory ex-Treg cell states in autoimmune settings and display type 2 helper T cell-like features during helminth infection. These cells exhibit transcriptional programs associated with proliferation, T cell activation and T helper differentiation, along with increased chromatin accessibility at regulatory regions enriched for key transcription factors controlling T cell activation and lineage specification. Mechanistically, Treg cell instability in the absence of TIF1γ is largely independent of transforming growth factor beta signaling and instead is driven by activation of the β-catenin pathway. TIF1γ-deficient Treg cells accumulate β-catenin and display enhanced TCF7 activity. Genetic or pharmacological targeting of β-catenin restores Treg cell stability and function. We identify TIF1γ as a critical regulator of Treg cell stability that restrains β-catenin-TCF7 signaling, thereby preserving Foxp3 expression and preventing inflammatory reprogramming.