A hallmark of anamniote vertebrate development is a window of embryonic transcription-independent cell divisions before onset of zygotic genome activation (ZGA). Chromatin determinants of ZGA are unexplored; however, marking of developmental genes by modified histones in sperm suggests a predictive role of histone marks for ZGA. In zebrafish, pre-ZGA development for ten cell cycles provides an opportunity to examine whether genomic enrichment in modified histones is present before initiation of transcription. By profiling histone H3 trimethylation on all zebrafish promoters before and after ZGA, we demonstrate here an epigenetic prepatterning of developmental gene expression. This involves pre-ZGA marking of transcriptionally inactive genes involved in homeostatic and developmental regulation by permissive H3K4me3 with or without repressive H3K9me3 or H3K27me3. Our data suggest that histone modifications are instructive for the developmental gene expression program. Display omitted Display omitted ► H3K4me3, H3K9me3, and H3K27me3 mark the zebrafish embryonic genome before ZGA ► The marked genes are transcriptionally silent and developmentally regulated ► A proportion of pre-ZGA H3K4me3- or H3K27me3-marked genes are also marked in sperm ► Pre-ZGA H3K4me3 marks predict a propensity for transcriptional activation after ZGA