Tetraploid (AABB) and hexaploid (AABBDD) wheat have multiple sets of similar chromosomes, with successful meiosis and preservation of fertility relying on synapsis and crossover (CO) formation only taking place between homologous chromosomes. In hexaploid wheat, the major meiotic geneTaZIP4-B2(Ph1) on chromosome 5B, promotes CO formation between homologous chromosomes, whilst suppressing COs between homeologous (related) chromosomes. In other species,ZIP4mutations eliminate approximately 85% of COs, consistent with loss of the class I CO pathway. Tetraploid wheat has threeZIP4copies:TtZIP4-A1on chromosome 3A,TtZIP4-B1on 3B andTtZIP4-B2on 5B. Here, we have developed single, double and triplezip4TILLING mutants and a CRISPRTtzip4-B2mutant, to determine the effect ofZIP4genes on synapsis and CO formation in the tetraploid wheat cultivar ‘Kronos’. We show that disruption of twoZIP4gene copies inTtzip4-A1B1double mutants, results in a 76-78% reduction in COs when compared to wild-type plants. Moreover, when all three copies are disrupted inTtzip4-A1B1B2triple mutants, COs are reduced by over 95%, suggesting that theTtZIP4-B2copy may also affect class II COs. If this is the case, the class I and class II CO pathways may be interlinked in wheat. WhenZIP4duplicated and diverged from chromosome 3B on wheat polyploidization, the new 5B copy,TaZIP4-B2, could have acquired an additional function to stabilize both CO pathways. In tetraploid plants deficient in all threeZIP4copies, synapsis is delayed and does not complete, consistent with our previous studies in hexaploid wheat, when a similar delay in synapsis was observed in a 59.3 Mb deletion mutant,ph1b, encompassing theTaZIP4-B2gene on chromosome 5B. These findings confirm the requirement ofZIP4-B2for efficient synapsis, and suggest thatTtZIP4genes have a stronger effect on synapsis than previously described in Arabidopsis and rice. Thus,ZIP4-B2in wheat accounts for the two major phenotypes reported forPh1, promotion of homologous synapsis and suppression of homeologous COs.