Post-translational chromatin modifications are an important regulatory mechanism in light signalling and circadian clock function. The regulation of diurnal transcript level changes requires fine-tuning of the expression of generally active genes depending on the prevailing environmental conditions. We investigated the association of histone modifications H3K4me3, H3K9ac, H3K9me2, H3S10p, H3K27ac, H3K27me3 and H3S28p with diurnal changes in transcript expression using chromatin immunoprecipitations followed by sequencing (ChIP-Seq) in fully expanded leaves 6 of Arabidopsis thaliana grown in short-day optimal and water-deficit conditions. We identified a differential H3K9ac, H3K27ac and H3S28p signature between end-of-day and end-of-night that is correlated with changes in diurnal transcript levels. Genes with this signature have particular over-represented promoter elements and encode proteins that are significantly enriched for transcription factors, circadian clock and starch catabolic process. Additional activating modifications were prevalent in optimally watered (H3S10p) and in water-deficit (H3K4me3) plants. The data suggest a mechanism for diurnal transcript level regulation in which reduced binding of repressive transcription factors facilitates activating H3K9ac, H3K27ac and H3S28p chromatin modifications. The presence of activating chromatin modification patterns on genes only at times of the day when their expression is required can explain why some genes are differentially inducible during the diurnal cycle.