The amplitudes of small-modifier protein signalling through ubiquitin and the Small Ubiquitin-like Modifiers, SUMO1-3, are critical to the correct phasing of repair protein accumulation, activity and clearance, and the completion of mammalian DNA double-strand break (DSB) repair. However, how SUMO-conjugate signalling in the response is delineated is poorly understood. At the same time, the role of the non-conjugated SUMO protein, SUMO4, has remained enigmatic. The data provides support of the differential presence of SUMO4 protein in different cell lines. Together with the data in the manuscript, the work reveals that SUMO4 is required to prevent excessive DNA-damage-induced SUMOylation and deleterious over-accumulation of RAP80. Mechanistically, the data shows SUMO4 acts independently of its conjugation and potentiates SENP1 catalytic activity. Together the data identify SUMO4 as a novel SUMO deconjugation component and that SUMO4:SENP1 are critical regulators of DNA-damage-induced SUMO signalling.