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Abstract Our sense of balance is among the most central of our sensory systems, particularly in the evolution of human positional behavior. The peripheral vestibular system (PVS) comprises the organs responsible for this sense; the semicircular canals (detecting angular acceleration) and otolith organs (utricle and saccule; detecting linear acceleration, vibration, and head tilt). Reconstructing vestibular evolution in the human lineage, however, is problematic. In contrast to considerable study of the canals, relationships between external bone and internal membranous otolith organs (otolith system) remain largely unexplored. This limits our understanding of vestibular functional morphology. This study combines spherical harmonic modeling and landmark-based shape analyses to model the configuration of the human otolith system. Our approach serves two aims: (1) test the hypothesis that bony form covaries with internal membranous anatomy; and (2) create a 3D morphometric model visualizing bony and membranous structure. Results demonstrate significant associations between bony and membranous tissues of the otolith system. These data provide the first evidence that external structure of the human otolith system is directly related to internal anatomy, suggesting a basic biological relationship. Our results visualize this structural relationship, offering new avenues into vestibular biomechanical modeling and assessing the evolution of the human balance system.