Migrasomes are essential intermediates for intercellular communication, involved in critical processes such as embryonic development, angiogenesis, and blood coagulation. So far, a comprehensive understanding of the protein cargoes within migrasomes and their transport mechanisms, which is fundamental to advancing the understanding of migrasomes function, is still lacking. In this study, we investigated the Rab-mediated cargo transport network to migrasomes. Rabs selectively transported proteins to migrasomes that are enriched in intracellular vesicle trafficking pathways. By integrating migrasomes protein profiling and Rab-effectors under various Rab activations, we identified key driving proteins involved in Rab-mediated cargo delivery to migrasomes. Additionally, we uncovered and validated that Rabs transported plasma membrane-localized receptors and matrix metalloproteinase to migrasomes, providing new insights into their in vivo functions. The proteomic dataset and integrated approach can be applied in further investigation of migrasomes in both physiological and disease contexts.