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Increasing wheat yield is essential in solving the global food shortage. The spikelet number per spike (SNS) is a primary factor that determines the kernel number per spike which has a great effect on wheat yield. Modern wheat breeding methods reduce the genetic diversity among cultivars, leading to a detrimental effect on future wheat production. It is, therefore, necessary to explore new genetic resources for SNS to increase wheat yield. A tetraploid landrace Ailanmai wild emmer wheat recombinant inbred line (RIL) population was used to construct a high-density genetic map using the wheat 55K single nucleotide polymorphism (SNP) array. The linkage map revealed that 94.83% (6204) of the mapped markers had consistent genetic and physical chromosomal locations. Fourteen quantitative trait loci (QTL) for SNS, explaining 4.23-27.26% of the phenotypic variation, were identified. QSns.sau-AM-2B.3 and QSns.sau-AM-3B.2 were detected as the major and novel QTL with a large cumulative effect that increased SNS by 17.47%. Some development-related genes within the physical intervals of QSns.sau-AM-2B.3 and QSns.sau-AM-3B.2 were predicted to participate in spikelet growth, thereby affecting SNS. Genetic associations between SNS and other agronomic traits such as a significant and positive correlation between SNS and thousand kernel weight (TKW) were detected and analyzed. QTL analysis was also performed for other spike-related traits, including spike length (SL), kernel number per spike (KNS), kernel number per spikelet (KNL), and spike density (SD). QSns.sau-AM-2B.3 was co-located with QSl.sau-AM-2B in the interval between AX-111626925 and AX-111588559. Similarly, QKns.sau-AM-5B.1 was co-related with QKnl.sau-AM-5B.2 in the region between AX-108760512 and AX-110180251. This study demonstrates the feasibility of wheat 55K SNP array in genetic mapping of tetraploid wheat population and shows the potential application of wheat related species in wheat improvement programs.