Metastatic spread of a cancer to secondary sites is a coordinated, non-random process. Cancer cell-secreted vesicles, especially exosomes, have recently been implicated in the guidance of metastatic dissemination, with their integrin composition determining some aspects of organ-specific localization. Nevertheless, whether the tumor microenvironment influences exosome biodistribution has yet to be investigated. Here, we show that cytokines present in the tumor microenvironment decorate cancer exosomes via binding to surface proteoglycans, causing exosome accumulation into specific cell lineages and distal organs. Cytokine-mediated exosome retention results in pre-metastatic niche formation within these organs, coupled with a higher metastatic burden. Strikingly, CCL2-decorated exosomes are mainly directed to a subset of cells that express the CCL2 receptor CCR2, demonstrating that exosome-bound cytokines are a novel and crucial determinant of exosome-cell interactions. Our results add a tumor microenvironmental aspect to the cancer cell-intrinsic mechanisms of organotropism identified thus far and will ultimately provide novel diagnostic and therapeutic tools to reduce the mortality associated with cancer metastasis.The fact that exosomes isolated from the blood of healthy subjects are also cytokine-conjugated, albeit displaying a different profile from exosomes isolated from cancer patients, further indicates that specific combinations of cytokines bound to exosomes could likewise affect other physiological and disease settings.