The petrosal anatomy and inner ear structure of Jurassic cladotherian mammals represent the ancestral morphological conditions (groundplan) from which modern therian mammals (marsupials and placentals) have evolved. We present the reconstruction of the petrosal and inner ear features of the Late Jurassic dryolestoid mammal Henkelotherium guimarotae from high-resolution computed tomography and three-dimensional imaging analysis. This study of Henkelotherium revealed a combination of derived and primitive features, including: cladotherian apomorphies, such as the promontorial sulcus for the internal carotid artery and reduced lateral trough; trechnotherian characters, such as an enclosed cochlear canaliculus for the perilymphatic duct, post-promontorial tympanic sinus and caudal tympanic process; in addition to plesiomorphic mammalian features, such as the cavum supracochleare and prootic canal. The inner ear of Henkelotherium shows a division between the utricle and saccule, a cochlear canal coiled through at least 270°, a distinctive primary bony lamina for the basilar membrane, and a secondary bony lamina. The development of the primary and secondary bony laminae in the cochlear canal is suggested here to be correlated with the concurrent coiling of the bony canal and membranous duct of the inner ear cochlea, apomorphies of the more inclusive cladotherian clade that also represent the ancestral morphotype of modern therian mammals. Because these features are crucial for high-frequency hearing in extant therian mammals, their early appearance in Late Jurassic cladotherians suggests a more ancient origination for high-frequency hearing in mammalian history than previously thought.