Salt stress is one of the most destructive environmental factors limiting crop growth and development. MicroRNAs (miRNAs) are a class of conserved endogenous small non-coding RNAs, playing the crucial role in regulating salt response and tolerance in plant. However, the miRNAs in wild emmer wheat, especially the key and specific salt-responsive miRNAs are not well studied. Here, we performed small RNA, transcriptome, and degradome sequencing of both of salt-tolerance (ST) and salt-sensitive (SS) wild emmer genotypes to identify the miRNA-mRNA modules associating with salt tolerance. Totally, 361 conserved known miRNAs and 414 novel miRNAs were identified in wild emmer, of which 93 salt-responsive miRNAs were found through comparative analysis of miRNA expression profiles. Combined with RNA-seq and degradome sequencing analysis, 224 miRNA-mRNA modules displayed the complete opposite expression trends between ST and SS genotypes, most of which functionally enriched into ROS homeostasis maintaining, osmotic pressure modulating, and root growth and development. Finally, the genetic variations of these miRNA-mRNA modules were investigated based on re-sequencing data of 91 accessions and then 222 signals associating with salt tolerance were identified through candidate-gene association studies. Particularly, a G to A variation in GSTU1 changed the cleavage site of tdi-miR9674a-p3, which significantly enhance the salt tolerance. This study reported the key and specific miRNA-mRNA modules associated with salt tolerance in wild emmer, which lay the foundation for improving the salt tolerance in cultivated emmer and bread wheat through miRNA engineering approach.