One defining goal of synthetic biology is the development of engineering-based approaches that enable the construction of gene-regulatory networks according to “design specs” generated from computational modeling 1– 6 . This approach provides a systematic framework for exploring how a given regulatory network generates a particular phenotypic behavior. Several fundamental gene circuits have been developed using this approach, including toggle switches 7 and oscillators 8– 10 , and these have been applied in novel contexts such as triggered biofilm development 11 and cellular population control 12 . Here we describe an engineered genetic oscillator in Escherichia coli that is fast, robust, and persistent, with tunable oscillatory periods as fast as 13 minutes. The oscillator was designed using a previously modeled network architecture comprising linked positive and negative feedback loops 1, 13 . Using a microfluidic platform tailored for single-cell microscopy, we precisely control environmental conditions and monitor oscillations in individual cells through multiple cycles. Experiments reveal remarkable robustness and persistence of oscillations in the designed circuit; almost every cell exhibited large-amplitude fluorescence oscillations throughout observation runs. The oscillatory period can be tuned by altering inducer levels, temperature, and media source. Computational modeling demonstrates that the key design principle for constructing a robust oscillator is a time delay in the negative feedback loop, which can mechanistically arise from the cascade of cellular processes involved in forming a functional transcription factor. The positive feedback loop increases the robustness of the oscillations and allows for greater tunability. Examination of our refined model suggested the existence of a simplified oscillator design without positive feedback, and we construct an oscillator strain confirming this computational prediction.