Placental dysfunction can lead to a variety of pregnancy pathologies, including intrauterine growth restriction (IUGR) and pre-eclampsia (PE). While these two conditions are distinct and can have differing outcomes for the mother and fetus, they share common molecular signatures. High levels of endoplasmic reticulum (ER) stress have been found in placentas from human cases and mouse models of IUGR and PE. The ER is a large organelle responsible for synthesis, maturation, and delivery of proteins essential for cellular function. ER stress occurs when misfolded proteins accumulate in the ER lumen. The cell responds with the conserved unfolded protein response and returns the ER to homeostasis by attenuating protein synthesis, activating transcriptional signaling cascades, and refolding or degrading misfolded proteins. ER stress can result in inflammation, cell death, and disease. The appearance of ER stress in the placenta does not occur in isolation and is accompanied by a variety of changes in maternal physiology. Inhibition of protein synthesis, reduced cell proliferation, or activation of pro-inflammatory pathways are all thought to be associated with differing levels of placental ER stress. This complex milieu makes it difficult to identify the direct effects of ER stress on placental and fetal health. To study the effects of the isolated ER stress response on the placenta, we used Tunicamycin to induce robust ER stress in E10.5 and E14.5 C57BL/6J mouse placentas. Because the response to ER stress involves thousands of gene expression changes, we used RNA-seq to measure the mRNA and small RNA changes associated with ER stress. We find that at each developmental time point, the placenta has a unique response to ER stress, with a specific associated ER stress response profile. We also find that the small RNA network reorganizes in ways that depend on both ER stress and on developmental time. Finally, small RNA expression changes appear to correlate with their targets under ER stress, and this correlation changes with development. Our data demonstrate that there is a complex regulation of mRNA and small RNA expression in the developing placenta, and ER stress impacts this regulatory network in profound ways. These results have important implications for potential roles of ER stress response in the pathophysiology of a variety of placental conditions.