The balance between plant growth and stress response is a key issue in the field of biology. In this process, mitogen-activated protein kinase 3 (MPK3) and MPK6 contribute to the construction of plants’ defense system during stress tolerance, while auxin, a growth-promoting hormone, is the key to maintaining plant growth. Nevertheless, the antagonistic or cooperative relationship between MPK3/6-mediated stress response and auxin-mediated plant growth remains unclear. Here, we demonstrate that stress-activated MPK3/6 interact with the auxin signaling repressors indoleacetic acid-induced protein 8 (IAA8) and IAA9, two key targets for regulating the auxin signaling output during stress responses. Protein phosphorylation mass spectrometry followed by a co-analysis with in vitro phosphorylation experiments revealed that MPK3/6 phosphorylated the S91, T94, and S152 residues of IAA8 and the S88 residue of IAA9. Phosphorylation significantly enhanced the protein stability of IAA8/9, thereby maintaining basal auxin signaling during plant stress adaptation. Collectively, MPK3/6-IAA8/9 are key modules that are turned on during plant stress adaptation to precisely reduce auxin signaling output, thereby preventing plants from improper vigorous growth under stress conditions.