Embryogenesis is remarkably robust to temperature variability, yet there is limited understanding of the homeostatic mechanisms that offset thermal effects during early development. Here, we measured the thermal acclimation response of upper thermal limits and profiled chromatin state and the transcriptome of D. melanogaster embryos (Bownes Stage 11) using single-nuclei multiome ATAC and RNA sequencing. We report that thermal acclimation, while preserving a common set of primordial cell types, rapidly shifted the upper thermal limit. Cool-acclimated embryos showed a homeostatic response characterized by increased chromatin accessibility at transcription factor binding motifs for the transcriptional activator Zelda, along with enhanced activity of gene regulatory networks in the primordial cell types including the foregut and hindgut, mesoderm, and peripheral nervous system. In addition, cool-acclimated embryos had higher expression of genes encoding ribosomal proteins and enzymes involved in oxidative phosphorylation. Despite the hypothesis that differential heat tolerance might be explained by differential expression of molecular chaperones, we did not observe widespread differences in the chromatin accessibility or expression of heat shock genes. Overall, our results suggest that environmental robustness to temperature during embryogenesis necessitates homeostatic gene expression responses that regulate the speed of development, potentially imposing metabolic costs that constrain upper thermal limits.