The mechanisms by which viruses hijack their host’s genetic machinery are of enormous current interest. One mechanism is adenosine diphosphate (ADP) ribosylation, where ADP-ribosyltransferases (ARTs) transfer an ADP-ribose fragment from the ubiquitous coenzyme nicotinamide adenine dinucleotide (NAD) to acceptor proteins. Here, we report that a bacteriophage T4 ART ModB surprisingly accept not only NAD but also NAD-capped-RNA as substrate, thereby covalently linking entire RNA chains to acceptor proteins in vitro and in vivo. We term this reaction an “RNAylation”. Salmonella ModB specifically RNAylates ribosomal proteins rS1 and rL2 at defined arginine residues, and a specific group of E. coli and T4 phage RNAs is linked to rS1 in vivo. T4 phages that express an inactive mutant of ModB show a decreased burst size and slowed lysis of E. coli. Our findings reveal a distinct biological role of NAD-RNA, namely activation of the RNA for enzymatic transfer to proteins. The attachment of specific RNAs to ribosomal proteins might provide a strategy for the phage to modulate the host’s translation machinery. This work exemplifies the first direct connection between RNA modification and post-translational protein modification. As ARTs play important roles far beyond viral infections, RNAylation may have far-reaching implications in the cellular context. Moreover, the discovery of the RNAylation might provide a starting point for the application of RNAylated-proteins as next-generation RNA therapeutics.