Plasticity enables organisms to extend their tolerance limits, but the physiological basis of plastic responses is not well characterized. Here, we demonstrate that Drosophila melanogaster embryos undergo rapid thermal acclimation, on the timescale of hours, that extends their upper thermal limit. Because early development is coordinated by changes in chromatin state and gene activation, we set out to characterize the molecular basis of embryonic thermal plasticity by performing single nuclei multiome ATAC and RNA sequencing. We found coordinated changes in chromatin state and the transcriptome in response to thermal acclimation. Cool-acclimated embryos exhibited thermal compensation through increased chromatin accessibility of transcription factor binding motifs of global transcriptional activators and higher expression of genes encoding ribosomal proteins and enzymes involved in oxidative phosphorylation. Although most of these shifts were common to all cell types, many changes were cell type specific. For example, cold-acclimated embryos had higher overall gene expression in tracheal primordial cells, presumably to prepare for increased gas exchange to support a higher metabolic rate. On the other hand, we observed modestly higher expression of genes involved in cell migration and cell adhesion in warm-acclimated embryos, particularly in ventral nerve cord primordia, suggesting a potential role for locomotor and sensory development in embryonic heat tolerance. Our results indicate that thermal plasticity is largely mediated by shifts in the epigenome and transcriptome that regulate the speed of development and that may impose metabolic costs that constrain upper thermal limits.