Mammalian 53BP1 and replication timing regulatory factor 1 (RIF1) protect DNA double-strand breaks (DSBs) against nucleolytic degradation through the recruitment of the REV7-SHLD1-SHLD2-SHLD3 (shieldin) and CTC1–STN1–TEN1 (CST) complexes.Mouse models deficient in downstream effectors of DSB protection have enabled the comparative assessment of defects in V(D)J recombination and class switch recombination (CSR).Regulation of DSB resection is crucial for CSR but dispensable for V(D)J recombination.The DSB protection function of mammalian 53BP1 does not explain the CSR defect severity associated with its deficiency.V(D)J recombination and CSR rely on the dynamic reconfiguration of Tcr/Ig loci that is contributed by cohesin-mediated loop extrusion.We propose that mammalian 53BP1 mediates pre- and post-break functions related to Tcr/Ig dynamics and DSB end-tethering, respectively, during the two recombination reactions. The dissection of the key molecular activities contributed by 53BP1 to antibody gene diversification exemplifies the importance of considering the repair of V(D)J and class switch recombination DNA double-strand breaks in their architectural genomic contexts. The investigation of the close interplay between Tcr/Ig loci dynamics and the repair of these programmed breaks can provide a deeper understanding of the molecular bases of humoral immune responses. The DNA double-strand break (DSB) repair factor 53BP1 has long been implicated in V(D)J and class switch recombination (CSR) of mammalian lymphocyte receptors. However, the dissection of the underlying molecular activities is hampered by a paucity of studies V(D)J and plurality of phenotypes (CSR) associated with 53BP1 deficiency. Here, we revisit the currently accepted roles of 53BP1 in antibody diversification in view of the recent identification of its downstream effectors in DSB protection and latest advances in genome architecture. We propose that, in addition to end protection, 53BP1-mediated end-tethering stabilization is essential for CSR. Furthermore, we support a pre-DSB role during V(D)J recombination. Our perspective underscores the importance of evaluating repair of DSBs in relation to their dynamic architectural contexts. The DNA double-strand break (DSB) repair factor 53BP1 has long been implicated in V(D)J and class switch recombination (CSR) of mammalian lymphocyte receptors. However, the dissection of the underlying molecular activities is hampered by a paucity of studies V(D)J and plurality of phenotypes (CSR) associated with 53BP1 deficiency. Here, we revisit the currently accepted roles of 53BP1 in antibody diversification in view of the recent identification of its downstream effectors in DSB protection and latest advances in genome architecture. We propose that, in addition to end protection, 53BP1-mediated end-tethering stabilization is essential for CSR. Furthermore, we support a pre-DSB role during V(D)J recombination. Our perspective underscores the importance of evaluating repair of DSBs in relation to their dynamic architectural contexts.