The nervous system likely evolved to control behavior. However, the earliest nerve nets were highly decentralized, raising questions about how such control was achieved. To explore this question, we study neural dynamics in Clytia hemisphaerica, a genetically accessible hydrozoan jellyfish. Despite lacking a centralized nervous system, Clytia has a complex behavioral repertoire that is modulated by internal states.1 Using historical electrophysiology results and newly acquired behavioral data, we created multiscale models of Clytia’s nervous system during the control of rhythmic swim contractions. Prior electrophysiological studies suggest that Clytia swim motor neurons (SMNs) are intrinsic pacemakers with subthreshold membrane oscillations that drive periodic spiking at the animal’s swim pulse frequency (~4 Hz).2 We adapted a model of parabolic bursting neurons to develop a single-cell Hodgkin-Huxley-like model of ~4 Hz intrinsic oscillatory activity in SMNs.3 Using bifurcation analysis, we showed that the subthreshold membrane oscillations could be dissociated from the spiking mechanisms, despite similarities in time scales, permitting a reduction of the model from its original five dimensions down to two. Next, to understand the degree of control Clytia exhibit over their swim rhythm, we acquired 24 hours of behavioral videos of “head-fixed” jellyfish and performed pose estimation by tracking tentacle bulbs. We found that Clytia swim pulses can vary significantly and continuously in their degree of asynchrony and asymmetry. Observation in freely swimming Clytia suggests that synchronous pulses drive straight swimming while asynchronous pulses permit turning, with the degree of straight swimming versus turning varying on long timescales. Using our two-dimensional oscillator model, we created a simple ring network in which transient and local asynchrony in activity can be induced. Together, our work provides a theoretical foundation for future exploration of how circuits of oscillators, the animal’s biomechanics, and the fluid environment interact to create flexible and adaptive swimming behavior.