The evolutionary assembly of the vertebrate bodyplan has been characterized as a long-term ecological trend toward increasingly active and predatory lifestyles, culminating in jawed vertebrates that dominate modern vertebrate biodiversity [1-8]. This contrast is no more stark than between the earliest jawed vertebrates and their immediate relatives, the extinct jawless, dermal armor-encased osteostracans, which have conventionally been interpreted as benthic mud-grubbers with poor swimming capabilities and low maneuverability [9-12]. Using computational fluid dynamics, we show that osteostracan headshield morphology is compatible with a diversity of hydrodynamic efficiencies including passive control of water flow around the body; these could have increased versatility for adopting diverse locomotor strategies. Hydrodynamic performance varies with morphology, proximity to the substrate, and angle of attack (inclination). Morphotypes with dorsoventrally oblate headshields are hydrodynamically more efficient when swimming close to the substrate, whereas those with dorsoventrally more prolate headshields exhibit maximum hydrodynamic efficiency when swimming free from substrate effects. These results suggest different hydrofoil functions among osteostracan headshield morphologies, compatible with ecological diversification and undermining the traditional view that jawless stem-gnathostomes were ecologically constrained [9-12] with the origin of jaws as the key innovation that precipitated the ecological diversification of the group [13, 14].