It remains unknown how developmental regulatory networks evolve, the predictability of their evolution, or to what degree laboratory evolution can be used to explore these processes. To address these questions, we have used experimental evolution to examine the bicoid (bcd) network in Drosophila, which is essential for anterior-posterior patterning in early embryos. This network can be synthetically perturbed by increasing the dosage of bicoid, which causes a posterior shift of the networks’ regulatory outputs and a decrease in fitness. To directly monitor network evolution across populations with two extra copies of Bicoid, we performed unbiased genome-wide mutagenesis, followed by experimental evolution. We find that the evolved populations have increased fitness, canalization of gene expression, and normalized cuticles after ten generations. Using a multi-omics approach across the evolved populations, we find that there are increases in embryo length associated with maternal changes in metabolism and ovariole development. Consistent with our observation in laboratory evolution, we find that a wild population with larger embryos similarly rescues progeny with increased bcd expression. Together, our results necessitate a broader view of regulatory network evolution at the system level, and such knowledge learned from experimental evolution can help predict evolutionary trends in nature.