Abstract Allotetraploid rapeseed ( Brassica napus L.) is highly susceptible to salt stress, a worldwide limiting factor that causes severe losses in seed yield. Genetic variations in the resistance against salt stress found in rapeseed genotypes emphasizes the complex response architecture. Westar is ubiquitously used as a major transgenic receptor, and ZS11 is widely grown as a high production and good quality cultivar. In this study, Westar was identified to outperform than ZS11 under salt stress. Through cell component isolation, non-invasive micro-test, X-ray energy spectrum analysis, and ionomic profiling characterization, pectin demethylation was found to be a major regulator for differential salt resistance between Westar and ZS11. Integrated analyses of genome-wide DNA variations, differentially expression profiling, and gene co-expression network identified BnaC9.PME47 , encoding pectin methyl esterase, as a positive regulator mainly responsible for salt stress resistance. BnaC9.PME47 , located in two reported QTLs regions for salt resistance, was strongly induced by salt stress and localized on the cell wall. Natural variation of the promoter regions conferred higher expression of BnaC9.PME47 in Westar than in other salt-sensitive rapeseed genotypes. Loss-of-function of AtPME47 resulted in the hypersensitivity of Arabidopsis plants to salt stress. This study facilitates a more comprehensive understanding of the differential morpho-physiological and molecular responses to salt stress and abundant genetic diversity in rapeseed genotypes, and the integrated multiomics analyses provide novel insights regarding the rapid dissection of quantitative trait genes responsible for nutrient stresses in plant species with complex genomes.