We recently described a previously unknown trans-tentorial venous system (TTVS) connecting venous drainage throughout the brain in humans. Prior to this finding, it was believed that the embryologic tentorial plexus regresses, resulting in a largely avascular tentorium. Our finding contradicted this understanding and necessitated further investigation into the development of the newly described TTVS. Herein we sought to investigate mice as a model to study the development of this system. First, using vascular casting and ex vivo micro-computed tomography (micro-CT), we demonstrate that this TTVS is conserved in adult mice. Next, using high-resolution magnetic resonance imaging (MRI), we found the primitive tentorial venous plexus in murine embryo at day 14.5. We also found that, at this embryologic stage, the tentorial plexus drains the choroid plexus. Finally, using vascular casting and micro-CT, we found that the TTVS is the dominant venous drainage in the early postnatal period (P8). Herein, we demonstrate that the TTVS is conserved between mice and humans and present a longitudinal study of its development. In addition, our findings establish mice as a translational model for further study of this newly described system and its relationship to intracranial physiology.