Regulatory T (Treg) cells suppress the development of inflammatory disease, but our knowledge of transcriptional regulators that control this function remains incomplete. Here we show that expression of Id2 and Id3 in Tregcells was required to suppress development of fatal inflammatory disease. We found that T cell antigen receptor (TCR)-driven signaling initially decreased the abundance of Id3, which led to the activation of a follicular regulatory T (TFR) cell-specific transcription signature. However, sustained lower abundance of Id2 and Id3 interfered with proper development of TFRcells. Depletion of Id2 and Id3 expression in Tregcells resulted in compromised maintenance and localization of the Tregcell population. Thus, Id2 and Id3 enforce TFRcell checkpoints and control the maintenance and homing of Tregcells. © 2014 Nature America, Inc. All rights reserved.