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Spikelet number per spike (SNS) is the primary factor that determines wheat yield. Common wheat breeding reduces the genetic diversity among elite germplasm resources, 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 genetic map using a wheat 55K single- nucleotide polymorphism (SNP) array. The linkage map containing 1,150 bin markers with a total genetic distance of 2,411.8 cm was obtained. Based on the phenotypic data from the eight environments and best linear unbiased prediction (BLUP) values, five quantitative trait loci (QTLs) for SNS were identified, explaining 6.71–29.40% of the phenotypic variation. Two of them, QSns.sau-AM-2B.2 and QSns.sau-AM-3B.2, were detected as a major and novel QTL. Their effects were further validated in two additional F2 populations using tightly linked kompetitive allele-specific PCR (KASP) markers. Potential candidate genes within the physical intervals of the corresponding QTLs were predicted to participate in inflorescence development and spikelet formation. Genetic associations between SNS and other agronomic traits were also detected and analyzed. This study demonstrates the feasibility of the wheat 55K SNP array developed for common wheat in the genetic mapping of tetraploid population and shows the potential application of wheat-related species in wheat improvement programs.