The transcription factor Foxp3 dominantly controls regulatory T (Treg) cell function, and only its continuous expression guarantees the maintenance of full Treg cell-suppressive capacity. However, transcriptional regulators maintaining Foxp3 transcription are incompletely described. Here, we report that high E47 transcription factor activity in Treg cells resulted in unstable Foxp3 expression. Under homeostatic conditions, Treg cells expressed high levels of the E47 antagonist Id3, thus restricting E47 activity and maintaining Foxp3 expression. In contrast, stimulation of Id3-deficient or E47-overexpressing Treg cells resulted in the loss of Foxp3 expression in a subset of Treg cells in vivo and in vitro. Mechanistic analysis indicated that E47 activated expression of the transcription factor Spi-B and the suppressor of cytokine signaling 3 (SOCS3), which both downregulated Foxp3 expression. These findings demonstrate that the balance of Id3 and E47 controls the maintenance of Foxp3 expression in Treg cells and, thus, contributes to Treg cell plasticity. Display omitted •Id3−/− Treg cells lose expression of Foxp3 upon stimulation•The balance of Id3 and E47 controls Foxp3 transcription in established Treg cells•High E47 activity increases Spib and Socs3 transcription in Treg cells•Spi-B and SOCS3 repress Foxp3 expression Stable Foxp3 expression is instrumental for Treg cell function. Rauch et al. found that the transcriptional regulator Id3 maintains Foxp3 transcription in established Treg cells by restricting E47 transcription factor activity. They suggest that a dynamic modulation of the Id3-E47 balance could transiently alter Treg cell function during immune responses.