The DNA damage response (DDR) protein 53BP1 protects DNA ends from excessive resection in G1, and thereby favors repair by nonhomologous end-joining (NHEJ) as opposed to homologous recombination (HR). During S phase, BRCA1 antagonizes 53BP1 to promote HR. The pro-NHEJ and antirecombinase functions of 53BP1 are mediated in part by RIF1, the only known factor that requires 53BP1 phosphorylation for its recruitment to double-strand breaks (DSBs). Here, we show that a 53BP1 phosphomutant, 53BP18A, comprising alanine substitutions of the eight most N-terminal S/TQ phosphorylation sites, mimics 53BP1 deficiency by restoring genome stability in BRCA1-deficient cells yet behaves like wild-type 53BP1 with respect to immunoglobulin class switch recombination (CSR). 53BP18A recruits RIF1 but fails to recruit the DDR protein PTIP to DSBs, and disruption of PTIP phenocopies 53BP18A. We conclude that 53BP1 promotes productive CSR and suppresses mutagenic DNA repair through distinct phosphodependent interactions with RIF1 and PTIP. Display omitted •The mechanisms by which 53BP1 promotes NHEJ and inhibits HR are distinct•PTIP and RIF1 separate 53BP1 functions in productive and mutagenic DNA repair•PTIP promotes genome instability in BRCA1-deficient cells by inhibiting DSB resection•PTIP is required for NHEJ of dysfunctional telomeres The DNA repair protein 53BP1 relies on two different cofactors to mediate its productive function in B cell class switching and its mutagenic function in BRCA1-deficient cells, raising the possibility of targeting one without disrupting the other.