Traumatic brain injury (TBI) manifests with reduced cerebral blood flow and heightened blood-brain-barrier (BBB) permeability, yet the underlying mechanisms remain elusive. This study explores the involvement of microvascular occlusions (mVOs) in the traumatic penumbra and their contribution to these processes. mVOs were visualized in C57BL/6 mice by systemic administration of super-bright 30 nm lipidic nanodroplets (LnDs) one hour following controlled cortical impact TBI. Brains were investigated by fluorescent confocal imaging and correlative light-electron microscopy (CLEM). Additionally, caveolin (Cav1) knockout mice (Cav1tm1Mls/J) and wildtype controls (WT) were used to investigate the mechanisms of BBB opening at the site of mVOs. Our findings demonstrate that 50% of mVOs correlated with the extravasation of albumin, fibrinogen, IgG, and LnDs within the traumatic penumbra. Immunohistochemistry revealed mVO components comprising erythrocytes, platelets, fibrin, and leukocytes, indicative of microthrombosis. The extravasation of blood-borne molecules positively correlated with cellular presence within mVOs (n=426 clots; R=0.31, p=0.02) and inversely with fibrin content (R=-0.64, p<0.001). Genetic deletion of Cav1 notably reduced LnD extravasation across the BBB compared to WT controls (n=5 animals per group, p=0.002). Furthermore, CLEM unveiled a dampening of transcytosis in Cav1-deficient mice. Our study shows the occurrence of microthrombosis in the traumatic penumbra, amplifying BBB permeability at mVO sites. Additionally, the caveolin transport system seems to be a prominent mediator in BBB opening. These insights propose a novel theranostic avenue targeting the traumatic penumbra, offering potential diagnostic and therapeutic interventions for traumatic brain injury.