Histone lysine methylation is a dynamic epigenetic regulator of eukaryotic transcription critical for development, differentiation and the cell's response to stress. Catalysed by methyltransferases and reversed by demethylases, methylation can activate or repress transcription depending on site and methylation state. Disruption of this system contributes to human diseases and histone-modifying enzymes are emerging therapeutic targets. Increasing evidence suggests that these enzymes themselves are regulated by kinase signalling, yet how most phosphorylation events modulate chromatin and cellular stress responses remains poorly understood. Using budding yeast, my research investigates phosphorylation-dependent regulation of the histone demethylase Rph1p, which removes di- and tri-methylation from H3K36. Rph1p has 39 phosphosites, most of which remain uncharacterised and lack known kinases. To address this, we used a combination of targeted and quantitative mass spectrometry, site directed mutagenesis, transcriptomics and biochemical assays. We identified seven sites on Rph1p upregulated under salt stress, with an enrichment for proline-adjacent sites. However, gross H3K36 methylation was unchanged under salt stress and in phosphorylation-deficient Rph1p mutants of stress-responsive sites, suggesting locus-specific regulation rather than genome-wide effects. Salt stress-responsive sites Ser412 and Ser689 were found to be functionally important, as phosphorylation-deficient mutants of these residues caused impaired growth under salt stress. Unexpectedly, neither mutant showed any change in protein profile under salt stress. However, the phosphorylation-deficient Rph1p-Ser689 mutant exhibited downregulation of 18 snRNAs during chronic stress, the majority of which guide rRNA methylation of the large ribosomal subunit. We also found that the osmotic stress-activated and proline-directed kinase, Hog1p, phosphorylates Rph1p at several salt stress-responsive sites in vitro, with evidence of redundant regulation in vivo. Together, these findings uncover a new regulatory axis linking the kinase signalling system to chromatin modulation and non-coding RNA expression.