Salinity is a major abiotic stress that is a global threat to crop production, including chickpea. This study focused on understanding the complex molecular mechanisms underlying salinity tolerance using comparative transcriptome analysis of tolerant (ICCV 10, JG 11) and sensitive (DCP 92-3, Pusa 256) chickpea genotypes in control and salt-stressed environments. A total of 530 million reads were generated from root samples of four genotypes using Illumina HiSeq-2500. A total of 21,698 differentially expressed genes (DEGs) were identified, of which 11,456 and 10,242 were up- and down-regulated, respectively, in comparative analysis. These DEGs were associated with crucial metabolic pathways, including hormone signaling, photosynthesis, lipid and carbohydrate metabolism, and cell wall biogenesis. Gene ontology (GO) examination revealed an enrichment of transcripts involved in salinity response. A total of 4257 differentially expressed GO terms were categorized into 64 functional groups; of which, GO terms like, integral component of membrane, organelle, and cellular anatomical entity were highly represented in tolerant genotypes under salt stress. Significant up-regulation of transcripts encoding potassium transporter family HAK/KUP proteins, MIP/aquaporin protein family, NADH dehydrogenase, pectinesterase, and PP2C family proteins occurred under salt stress. The tolerant lines (ICCV 10 and JG 11) engaged highly efficient machinery in response to elevated salt stress, especially for signal transduction, transport and influx of K+ ions, and osmotic homeostasis. The overall study highlights the role of potential candidate genes and their regulatory networks which can be utilized in breeding salt tolerant chickpea cultivars.