Genes direct cells into unique and diverse lineages and identities where they carry out biological functions required to support organismal complexity. Aim. The purpose of this study was to elucidate chromatin dynamics underlying genes controlling lineage decisions and cell identity. Methods. We analyzed cardiac and vascular lineages derived from hPSCs by ChIP-seq for H3K4me3 (open chromatin) to elucidate the relationship between chromatin methylation dynamics and the biological function of genes in cardiovascular development. ChIP-seq data were analyzed by an unbiased genome-wide screening approach in which H3K4me3 peak shapes were compared in a pairwise manner to generate dendrograms of peaks grouped based on similarity of shape (height, width, and modality). Results. These data revealed significantly different H3K4me3 domain shapes that uniquely mark gene groups governing specific biological functions. We focused on H3K4me3 chromatin domain shapes unique to genes governing cell identity and tested its broader applicability using histone methylation data from greater than 100 cell and tissue types. Out of the greater than ten thousand genes marked by H3K4me3 in cells, our unbiased H3K4me3 screening algorithm enriched for cell type specific identity genes like transcription factors and cell-type specific non-coding RNAs that were selected independent of any gene expression information. The same algorithm was used to analyze genome-wide chromatin domain shapes of histone 3 K36me3, K27me3, K9me3, K27ac, and K4me1 all of which failed to enrich for cell identity genes. This data reveals unique features of H3K4me3 peak shape as a means to identify genes and non-coding RNAs governing cell type specific biological functions independent of any other chromatin mark or expression data. Conclusion. Taken together, we have identified an unbiased genome-wide screening approach of open chromatin as a means to enrich for protein-coding and non-coding transcripts underlying cell identity that can be used to elucidate the genetic basis of lineage decisions and cell states in health and disease.