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Wheat powdery mildew (<i>Blumeria graminis</i> f. sp. <i>tritici</i>, <i>Bgt</i>, recently clarified as <i>B. graminis</i> s. str.), is one of the most destructive diseases of wheat. <i>Pm60</i> is a nucleotide-binding leucine-rich repeat (NLR) gene that confers race-specific resistance to <i>Bgt</i>. Allelic variants (<i>Pm60</i>, <i>Pm60a</i>, and <i>Pm60b</i>) were found in <i>Triticum urartu</i> and <i>T. dicoccoides</i>, the wild progenitors of wheat. In the present study, we studied the diversity of the <i>Pm60</i> locus in a large set of wheat germplasm and found 20 tetraploid wheats harboring the <i>Pm60</i> alleles, which correspond to three novel haplotypes (HapI–HapIII). HapI (<i>Pm60</i> allele) and HapII (<i>Pm60a</i> allele) were present in domesticated tetraploid wheats, whereas HapIII (<i>Pm60a</i> allele) was identified in wild tetraploid <i>T. araraticum</i>. A sequence comparison of HapII and HapIII revealed that they differed by three SNPs and a GCC deletion. Results of the phylogenetic analysis revealed that HapII was more closely related to the functional haplotype <i>MlIW172</i>. Infection tests showed that HapII-carrying lines display a partial resistance response to <i>Bgt#GH</i>, while HapI was susceptible. Our results provide insights into the genetic evolution of the <i>Pm60</i> locus and potential valuable alleles for powdery mildew resistance breeding.