Oncolytic viruses (OV) preferentially infect tumor cells and activate the anti-tumor immune response. OV can also be engineered to express therapeutic transgenes to support oncolytic activity. Extracellular vesicles (EV) are produced by all cell types and mediate intercellular communication. Tumor EV modulate the activity of both neighboring and distant cells, and are involved in multiple phenomena such as immunosuppression. Viruses are strong inducers of EV secretion but little is known about tumor EV during oncolytic infection. In this study, we aimed at understanding how OV alter the secretion and functions of tumor EV. We infected human melanoma and thoracic cancer cell lines with different OV (poxviruses, paramyxoviruses, rhabdoviruses). After isolation by differential ultracentrifugation, we characterized EV in terms of concentration (tunable resistive pulse sensing), morphology (electron microscopy) and protein content (mass spectrometry, proteinase protection assay). We used a CRE-based recombination system to evaluate the release of functional EV cargo into recipient cells. We show that EV secreted from infected tumor cells are more abundant. They harbor proteins typical of EV and are spontaneously loaded with proteins of viral origin. EV mimicking those from infected cells transfer their content to recipient cells more readily than those from uninfected cells. We show that different OV increase tumor EV secretion and alter their content. Our data suggest that EV-mediated intercellular communication in the tumor could be enhanced by oncolytic infection. This could have a functional impact on the tumor microenvironment.