Caveolin-1 (CAV1) is a structural protein of caveolae that function as sensors of plasma membrane stress. In advanced prostate cancer, CAV1 is overexpressed but fails to form caveolae due to the loss of the caveolar co-factor Cavin-1. Cavin-1 expression in prostate cancer cells attenuated growth and metastasis. Mechanistically, Cavin-1 expression led to caveolae formation, altered lipid raft membrane distribution and protein composition, as well as secretion of selected proteins and microRNA (miRNA) via extracellular vesicles (EVs). Specifically, Cavin-1 suppressed the EV level of oncogenic miR-148a without altering its total cellular level. As Cavin-1 impacts EV protein and miRNA composition, we hypothesized the involvement of specific RNA-binding proteins in miRNA EV export. Small RNA sequencing revealed that Cavin-1 expression lead to the differential export of 19 out of 95 EV miRNAs. Subcellular proteomics, protein-protein interaction network and functional annotation analysis revealed 5 candidate RNA-binding proteins. Out of these, only heterogeneous nuclear Ribonucleoprotein K (hnRNPK) is known to bind the AGUGCA sequence motif identified in 12 out of 19 selectively exported miRNAs, including the oncogenic miR-148a. To support the computational results, we show that hnRNPK and miR-148a co-localize in cytoplasmic puncta in PC3 cells. hnRNPK partially co-localize with CD9, a marker of multivesicular bodies from which exosome-type EVs originate. Strikingly, Cavin-1 expression leads to the redistribution of hnRNPK to the endoplasmic reticulum, providing a mechanisms for reduced secretion of hnRNPK and target miRNAs. Taken together, our results suggest a non-canonical function of Cavin-1, in regulating the trafficking of RNA-binding proteins such as hnRNPK, enabling the selective export of miRNAs to exosomes. While hnRNPK is commonly detected in cancer derived EVs, this is the first study to reveal a link between hnRNPK and selective miRNA export.