The mitochondrial sheath is a key requirement for sperm function, providing structural support and the energy necessary for motility. While many of the key steps of sperm mitochondrial sheath formation have been described at a cytological level, the molecular processes required for its assembly and function remain poorly understood. Recently, poorly characterised coiled coil domain containing protein, CCDC112, has been identified as a likely regulator of cilia and sperm tail formation via roles in the assembly, maintenance, and remodelling of the centrosome. Herein, using a Ccdc112 loss-of-function mouse model, we tested this role and show that CCDC112 is essential for male fertility. We demonstrated a critical role for CCDC112 in mitochondrial morphogenesis and remodelling during mitochondrial sheath formation, where loss of CCDC112 resulted in sperm with highly abnormal mitochondrial sheath architecture and stiffened midpieces with limited flexibility (p <0.0001 compared to wildtype). Consequently, loss-of-function sperm possessed an irregular flagellar waveform, with significantly diminished mitochondrial ATP production and mechanical power, resulting in a significantly reduced ability for progressive motility and swimming speed. Ultimately, given their inability to sufficiently traverse the female reproductive tract, loss-of-function sperm exhibit reduced fertilisation capabilities, with impaired penetration of the zonae pellucidae of oocytes and poor sperm-oocyte fusion. We identified that these defects were in part explained by CCDC112 acting as a component of the distal appendages of the mother centriole. Using this mouse model, we also identified a previously unrecognised process of epididymal mitochondrial sheath maturation that occurs during epididymal sperm maturation. These findings suggest that upon sperm release from the testis, most sperm midpieces are structurally immature, with maturation continuing as sperm transit through the epididymis from caput to cauda. Collectively, we show that CCDC112 is an essential regulator of sperm midpiece assembly and function and reveal a novel form of epididymal sperm maturation.