Extracellular vesicles (EVs) laden with protein and genetic cargo are released by cells for the purpose of intercellular communication. In the case of pathogens, such as the malaria parasite Plasmodium falciparum (Pf), EVs are utilized to promote parasitic growth and alter the host’s response. We found that while growing inside human red blood cells, Pf secretes EVs containing RNA, genomic DNA and even an assembled and functional 20S proteasome complex to modify different host systems. We further showed that this parasite’s EVs also transfer three Pf transcripts belonging to the ETRAMP family and that, surprisingly, these transcripts are rapidly imported into the nucleus of human monocytes upon EV internalization. These findings open a new direction of investigation in parasite-host communication: exploring fascinating virulence-promoting strategies of the malaria parasite.