Various histone modifications, including acetylation and methylation, are widely associated with gene transcription, but their functional importance at individual genes, and the extent to which they are selectively employed remains unclear. Here, we identify widespread differences in genome-wide patterns of two prominent marks, H3K9ac and H3K4me3, in budding yeasts. In addition to distinct gene profiles, their relative abundance varied considerably, irrespective of expression. Interestingly, these differences could be associated with several attributes, in particular, nucleosome organization, expression variability and gene essentiality. Higher acetylation was enriched at non-essential, responsive and OPN genes, while higher methylation was more prevalent at essential, periodically expressed and DPN genes. We considered that these biases enable disparate strategies of transcription that is, H3K9ac may engender variability, and H3K4me3, stability. To evaluate these notions, we examined their evolutionary divergence between closely related yeast species. Although individually well conserved at orthologous genes, changes between modifications were mostly uncorrelated, suggesting largely non-overlapping genetic regulation. Importantly, methylation was significantly better at explaining expression divergence: H3K4me3 levels were well coordinated at both invariant and divergently expressed genes, but H3K9ac changes often occurred in the absence of expression changes. Taken together, our results strongly support selective utilization of histone modifications at individual genes H3K4 tri-methylation may serve in evolution to stabilize average expression at appropriate levels, whilst H3 acetyl marks govern more indirect aspects, such as transcription initiation.