Since the discovery of the first DNA damage-induced histone modification by Bill Bonner in 1998, we know that DNA double strand breaks (DSBs) trigger accumulation of proteins that read these modifications and navigate repair pathways to restore DNA integrity with high fidelity and with minimum collateral damage to healthy genome. Although the recent addition of shieldin on the list of proteins that carry out this function was a major step forward, we are still lacking a unifying concept to explain how this vital mode of genome maintenance operates in three-dimensional (3D) space of mammalian nucleus. The conundrum is that while active sites of DNA repair are confined to tiny nuclear volumes, the accompanying chromatin responses spread out to megabase distances. Despite this has been noticed already two decades ago in the Bonner study, we do not understand how repair reactions benefit from remote chromatin modifications. Likewise, we do not know how these modifications reflect, and impact on, chromatin architecture. Furthermore, the abundance of chromatin-bound genome caretakers can vary by an order of magnitude for reasons that remain unclear. To answer these questions, we applied super-resolution microscopy to interrogate spatio-temporal chromatin features after DNA breakage. We will provide evidence that chromatin architecture at DSB sites is actively stabilized and that topological integrity of DSB-flanking chromatin lays down a physical fundament for repair fidelity. We will support this by showing that 53BP1 and RIF1, two proteins that sequentially accumulate at DSB sites, form an autonomous functional module that actively maintains globular chromatin structure. We will show that depletion of 53BP1 or RIF1 phenocopies malfunction of cohesin, the key organizer or chromatin architecture, by causing distortion of chromatin topology accompanied by DSB hyperresection. Unexpectedly, we will also show that stabilization of higher-order chromatin structure after DNA breakage operates independently of repair. We will integrate these findings to a conceptual framework suggesting that 53BP1 and RIF1 primarily evolved to safeguard information stored in 3D chromatin and only later were harnessed to foster repair fidelity by locally concentrating ultralow-abundant antagonists of DSB resection such as shieldin.