To maintain immune tolerance, effector T‐cell (Teff) responses must be checked by the regulatory T cells (Tregs) in time. It remains incompletely understood how Tregs sense real‐time Teff activation. Here, we report that the AP‐1 transcription factor JunB, which is induced in Teffs upon T‐cell receptor (TCR) activation, is also increased in Tregs by TCR stimuli. Treg‐specific deletion of Junb impairs Treg identity, causes uncontrolled inflammatory cytokine production by Teffs and leads to the T‐box transcription factor T‐bet‐dependent spontaneous inflammation. Furthermore, JunB deficiency in Tregs unleashes antitumor Teff responses in a mouse model of melanoma. We conclude that JunB alarms Tregs of the emerging Teff activation and synchronizes immune regulation with the immune reaction in autoimmunity and cancer.