Viruses modulate ecosystems by directly altering host metabolisms through auxiliary metabolic genes, which are obtained through random sampling of the host genome and rise to fixation, presumably through improved viral fitness by alleviating key metabolic bottlenecks during infection. Conspicuously, however, viral genomes are not known to encode the core components of translation machinery, such as ribosomal proteins (RPs), though genes for RPs S1 and S21 have been detected in viral metagenomes. Here we augment this little-noticed observation using available reference genomes, global-scale viral metagenomic datasets, and functional assays for select proteins. We identify 15 different RPs across diverse viral genomes arising from cultivated viral isolates (5 RPs in 16 genomes) and metagenome-assembled viruses (14 RPs in 1,403 uncultivated virus genomes). Among these, S21 and L7/L12 are the most common, and functional assays show that both proteins are incorporated into 70S ribosomes when expressed in Escherichia coli, indicating that they might modulate protein translation during infection. Ecological distributions of virus-encoded RPs suggest ecosystem-specific virus adaptations, whereby aquatic viruses appear to selectively incorporate genes for S21, L31 and L33, whereas S6, S9, S15 and S30AE genes are enriched among viruses infecting animal-associated bacteria. Finally, the fact that viruses tend to encode dynamic RPs, suggests that the viral proteins likely replace cellular versions in host ribosomes, likely enabling takeover of host translational machinery.