Throughout the life cycle, the functional specializations of cells and tissues are directly reflected in the patterns of chromatin structure. During embryogenesis, genetic loci involved in cell fate specification and differentiation –committed decisions that restrict a cell’s developmental potential– must be packaged in such a way that they can ultimately respond to precise spatial and temporal developmental cues. Furthermore, a mechanism must exist for faithfully replicating such chromatin states in daughter cells following mitosis. We have measured by ATAC-seq how the initial patterns of chromatin structure are established and maintained during early Drosophila embryogenesis with three-minute time resolution for the three cell cycles preceding the midblastula transition (MBT). During this period, the embryo undergoes large-scale zygotic genome activation, and initiates the process of pattern formation. However, because such embryos are also simultaneously engaged in mitotic nuclear amplification, one longstanding question has been to what extent stable chromatin structure could be established in the context of an extremely rapid cell cycle. We find that extensive heritable chromatin structure can be established under these conditions. Over this period, thousands of genomic loci acquire chromatin accessibility at specific times, in response to different biological timing mechanisms. Enhancers, for example, are accessible from very early in development, whereas the majority of promoters acquire accessibility at or around the MBT. The majority of these promoters gain accessibility in response to the biological timer that measures the nucleo-cytoplasmic ratio and controls the onset of the MBT. In addition, we observe that once established, these patterns of accessibility are maintained in metaphase chromatin, suggesting that the major mechanism for epigenetic inheritance of embryonic chromatin structure relies on acquisition of mitotic stability or chromatin “bookmarking”.