Dynamic SUMO modifications of diverse cellular protein groups are critical to orchestrate resolution of stresses such as genome damage, hypoxia or proteotoxicity. Defense against pathogen insult (usually reliant upon host recognition of ‘non-self’ nucleic acids), is also modulated by SUMO, but the underlying mechanisms are incompletely understood. Here, we used quantitative SILAC-based proteomics to survey pan-viral host SUMOylation responses, creating a resource of almost 600 common and unique SUMO remodeling events that are mounted during influenza A and B virus infections, as well as during viral immune stimulation. By integrating knock-out/reconstitution models and transcriptomics, we provide evidence that influenza virus triggered loss of SUMO-modified TRIM28 leads to derepression of endogenous retroviral elements, unmasking this cellular pool of ‘self’ double-stranded (ds) RNA. Consequently, loss of SUMO-modified TRIM28 potentiates canonical cytosolic dsRNA-activated interferon-mediated defenses. Our data suggest that a key nuclear mechanism that prevents expression of endogenous retroviruses has been functionally co-opted via a stress-induced SUMO switch to augment antiviral immunity.