Embryonic development combines paradoxical properties: it has great precision, it is usually conducted at breakneck speed and it is flexible on relatively short evolutionary time scales, particularly at early stages. While these features appear mutually exclusive, we consider how they may be reconciled by the properties of key early regulatory networks. We illustrate these ideas with the network that controls development of endoderm progenitors. We argue that this network enables precision because of its intrinsic stability, self propagation and dependence on signalling. The network enables high developmental speed because it is rapidly established by maternal inputs at multiple points. In turn these properties confer flexibility on an evolutionary time scale because they can be initiated in many ways, while buffering essential progenitor cell populations against changes in their embryonic environment on both evolutionary and developmental time scales. Although stable, these networks must be capable of rapid dissolution as cell differentiation progresses. While we focus on the core early endodermal network of vertebrates, we argue that these properties are likely to be general in early embryonic stem cell populations, such as mammalian ES cells. BioEssays 30:757–765, 2008. © 2008 Wiley Periodicals, Inc.