Abstract The evolutionary transition to powered flight remains controversial in bats, the only flying mammals. We applied aerodynamic modeling to reconstruct flight in the oldest complete fossil bat, the archaic Onychonycteris finneyi from the early Eocene of North America. Results indicate that Onychonycteris was capable of both gliding and powered flight either in a standard normodense aerial medium or in the hyperdense atmosphere that we estimate for the Eocene from two independent palaeogeochemical proxies. Aerodynamic continuity across a morphological gradient is further demonstrated by modeled intermediate forms with increasing aspect ratio (AR) produced by digital elongation based on chiropteran developmental data. Here a gliding performance gradient emerged of decreasing sink rate with increasing AR that eventually allowed applying available muscle power to achieve level flight using flapping, which is greatly facilitated in hyperdense air. This gradient strongly supports a gliding (trees-down) transition to powered flight in bats.