Migrasomes, vesicular organelles generated on the retraction fibers of migrating cells, play a crucial role in migracytosis, mediating intercellular communication. The content cargoes determine the functional specificity of migrasomes. Migrasomes harbor numerous intraluminal vesicles, a pivotal component of their cargo. The mechanism underlying the transportation of these intraluminal vesicles to the migrasomes remain enigmatic. In this study, we identified a pathway by which Rab10-Caveolin1 mediates the transport of intraluminal vesicles to migrasomes. This intricate process necessitates the coordination of the motor protein Myosin Va, adaptor proteins RILPL2, facilitating vesicle transportation through retraction fibers to the migrasomes. Notably, the phosphorylation of Rab10 by the kinase LRRK2 augments this transport. Moreover, CSF-1 is selectively transported to migrasomes through this mechanism, subsequently fostering monocyte-macrophage differentiation in skin wound healing, which adds to our understanding of the physiological role of migrasomes.