Salt stress has devastating effects on agriculture, yet the key regulators modulating the transcriptional dynamics of salt-responsive genes remain largely elusive in plants. Here, we discover that salt stress substantially induces the kinase activity of Mediator cyclin-dependent kinase 8 (CDK8), which is essential for its positive role in regulating salt tolerance. CDK8 is identified to phosphorylate AT-hook motif nuclear-localized protein 10 (AHL10) at serine 314, leading to its degradation under salt stress. Consistently, AHL10 is found to negatively regulate salt tolerance. Transcriptome analysis further indicates that CDK8 regulates over 20% of salt-responsive genes, half of which are co-regulated by AHL10. Moreover, AHL10 is revealed to recruit SU(VAR)3-9 homologs (SUVH2/9) to AT-rich DNA sequences in the nuclear matrix-attachment regions (MARs) of salt-responsive gene promoters, facilitating H3K9me2 deposition and repressing salt-responsive genes. Our study thereby has identified the CDK8-AHL10-SUVH2/9 module as a key molecular switch controlling transcriptional dynamics in response to salt stress.