Insects determine their body segments in two different ways. Short-germband insects, such as the flour beetle Tribolium castaneum, use a molecular clock to establish segments sequentially. In contrast, long-germband insects, such as the vinegar fly Drosophila melanogaster, determine all segments simultaneously through a hierarchical cascade of gene regulation. Gap genes constitute the first layer of the Drosophila segmentation gene hierarchy, downstream of maternal gradients. We use data driven modelling and phase space analysis to show that shifting gap domains in the posterior half of the Drosophila embryo are an emergent property of a robust damped oscillator mechanism. The rate at which gap domains shift is determined by the level of maternal Caudal (Cad), which also regulates the frequency of the Tribolium molecular clock. Our evidence indicates that the regulatory dynamics underlying long- and short-germband segmentation are much more similar than previously thought. This similarity may help explain why long-germband segmentation evolved convergently multiple times during the radiation of the holometabolan insects.