Salinity is a major abiotic stress that causes substantial agricultural losses worldwide. Chickpea (Cicer arietinum L.) is an important legume crop but is salt-sensitive. Previous physiological and genetic studies revealed the contrasting response of two desi chickpea varieties, salt-sensitive Rupali and salt-tolerant Genesis836, to salt stress. To understand the complex molecular regulation of salt tolerance mechanisms in these two chickpea genotypes, we examined the leaf transcriptome repertoire of Rupali and Genesis836 in control and salt-stressed conditions. Using linear models, we identified categories of differentially expressed genes (DEGs) describing the genotypic differences: salt-responsive DEGs in Rupali (1,604) and Genesis836 (1,751) with 907 and 1,054 DEGs unique to Rupali and Genesis836, respectively, salt responsive DEGs (3,376), genotype-dependent DEGs (4,170), and genotype-dependent salt-responsive DEGs (122). Functional DEG annotation revealed that the salt treatment affected genes involved in ion transport, osmotic adjustment, photosynthesis, energy generation, stress and hormone signalling, and regulatory pathways. Our results showed that while Genesis836 and Rupali have similar primary salt response mechanisms (common salt-responsive DEGs), their contrasting salt response is attributed to the differential expression of genes primarily involved in ion transport and photosynthesis. Interestingly, variant calling between the two genotypes identified SNPs/InDels in 768 Genesis836 and 701 Rupali salt-responsive DEGs with 1,741 variants identified in Genesis836 and 1,449 variants identified in Rupali. In addition, the presence of premature stop codons was detected in 35 genes in Rupali. This study provides valuable insights into the molecular regulation underpinning the physiological basis of salt tolerance in two chickpea genotypes and offers potential candidate genes for the improvement of salt tolerance in chickpeas.