Cognitive functions for navigation and memory rely on emergent properties of neural ensembles in the hippocampus, such as activity replay1–5 and theta sequences6–9. Yet, whether and how these phenomena generalize across species with distinct navigational demands and neurophysiological properties remain unclear. Here, we wirelessly recorded neural activity from large populations of cells and local field potentials (LFPs) from the hippocampus of freely flying bats engaged in free, spontaneous foraging behavior. During rest, we identified time-compressed forward and reverse replay of multiple flight trajectories coinciding with sharp-wave ripples (SWRs). Yet, replays occurred predominantly at locations that were both spatially and temporally distant from the replayed behavior, and their speed scaled with trajectory length, challenging existing models of replay mechanisms. During flight, neural ensembles exhibited fast representational sweeps, where the decoded location cyclically moved ahead of the bat’s position. In contrast to reports in rodents, sweeps occurred in the absence of theta oscillations and were instead phase-locked to a prominent motor behavioral rhythm - the bat’s wingbeat cycle. This suggests that behaviorally-relevant sensorimotor rhythms can interact with hippocampal ensemble dynamics in a highly structured manner. Combined, our findings challenge existing models of ensemble dynamics in the mammalian hippocampus and highlight the importance of comparative studies under ethologically relevant conditions for elucidating brain function.