Bacteriophages and their bacterial hosts engage in an evolutionary arms race, developing intricate attack and defense mechanisms. Here, we employ state-of-the-art quantitative phosphoproteomics to uncover a previously uncharacterized mechanism by which phage T7 manipulates host defenses. We demonstrate that the T7 protein kinase (T7K) induces a massive wave of phosphorylation of both host and phage proteomes during infection, modifying over 70% of detected proteins. This unprecedented scale of phosphorylation far exceeds the number of previously known phosphorylation events in E. coli, and also the promiscuity of any protein kinase reported to date. Stoichiometry analysis reveals a striking bias towards nucleic acid-binding substrates, which we show is mediated by a DNA-binding domain within T7K. The promiscuous yet targeted activity allows T7K to modulate multiple host defense systems simultaneously. We provide insights into how T7K weakens the Retron-Eco9 and DarTG1 bacterial defense systems through specific phosphorylation events, and demonstrate that phosphomimetic mutations in key sites completely deactivate their ability to defend. Furthermore, by screening a diverse natural isolate strain collection as well as E. coli K12 armed with plasmid-encoded defense systems, we demonstrate the prevalence and significance of T7K-mediated defense system interactions in nature. Our findings reveal a novel, broadly-acting phage counter-defense strategy and underscore the importance of post-translational modifications in phage-host interactions.