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The genetic circuitry that encodes the developmental programme of mammals is regulated by transcription factors and chromatin modifiers. During early gestation, the three embryonic germ layers are established in a process termed gastrulation. The impact of deleterious mutations in chromatin modifiers such as the polycomb proteins manifests during gastrulation, leading to early developmental failure and lethality in mouse models. Embryonic stem cells have provided key insights into the molecular function of polycomb proteins, but it is impossible to fully appreciate the role of these epigenetic factors in development, or how development is perturbed due to their deficiency, in the steady-state. To address this, we have employed a tractable embryonic stem cell differentiation system to model primitive streak formation and early gastrulation. Using this approach, we find that loss of the repressive polycomb mark H3K27me3 is delayed relative to transcriptional activation, indicating a subordinate rather than instructive role in gene repression. Despite this, chemical inhibition of polycomb enhanced endodermal differentiation efficiency, but did so at the cost of lineage fidelity. These findings highlight the importance of the polycomb system in stabilising the developmental transcriptional response and, in so doing, in shoring up cellular specification. Author summary: Embryogenesis requires a tightly coordinated programme of cellular expansion and specialisation to gives rise to all of the cell- and tissue-types of the developing organism. In mammals this is controlled, in part, by chromatin modifications that help to establish the underlying gene expression patterns. However, limited numbers of cells make it hard to study these mechanisms directly in embryos. To overcome this, we employed a defined cell-differentiation system to experimentally model early embryonic development. Using this, in combination with pharmacological and genetic approaches, we identified DNA sequences with the potential to act as control switches at developmentally regulated genes. Surprisingly, we did not detect any loss of the polycomb-associated chromatin mark H3K27me3, despite evident transcriptional activation within the pool of cells. However, blocking deposition of this mark enhanced differentiation, but also led to reduced developmental fidelity due to increased production of inappropriate cell types. This demonstrated that, although acting as a secondary layer of gene regulation, polycomb marks are essential to stabilise developmental gene expression patterns and shore up cellular specification. [ABSTRACT FROM AUTHOR]