Drosophila segmentation is mediated by a group of periodically expressed transcription factors known as the pair-rule genes. These genes are expressed dynamically, with many transitioning from double segment periodicity to single segment periodicity at gastrulation. The myriad cross-regulatory interactions responsible for these expression changes have been studied for over 30 years, however a systems level understanding of pair-rule patterning is still lacking. We carefully analysed the spatiotemporal dynamics of pair-rule gene expression, and found that frequency-doubling is precipitated by multiple coordinated regulatory changes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa), as the cause of these changes, and propose a new model for the patterning of the even-numbered parasegment boundaries, which relies on Opa-dependent regulatory interactions. Our findings indicate that the pair-rule gene regulatory network has temporally-modulated topology and dynamics, permitting stage-specific patterning roles.