Two markers on Chromosome 2 of chickpea (Cicer arietinum) are reportedly associated with resistance to race 4 Fusarium wilt, and are frequently used in breeding. However, the genes in this region that actually confer wilt resistance are unknown. We aimed to characterise them using both in silico approaches and marker trait association (MTA) analysis. Of the 225 protein-encoding genes in this region, 51 showed significant differential expression in two contrasting chickpea genotypes under wilt, with potential involvement in stress response. From a diverse set of 244 chickpea genotypes, two sets of 40 resistant and 40 susceptible genotypes were selected based on disease incidence and amplification pattern of the TA59 marker. All cultivars were further genotyped with 1238 single nucleotide polymorphisms (SNPs) specific to the 51 genes; only seven SNPs were significantly correlated with disease. SNP Ca2_24099002, specific to the LOC101498008 (Transmembrane protein 87A) gene, accounted for the highest phenotypic variance for disease incidence at 16.30%, whereas SNPs Ca2_25166118 and Ca2_27029215, specific to the LOC101494644 (β-glucosidase BoGH3B-like) and LOC101505289 (Putative tRNA pseudouridine synthase) genes, explained 10.51% and 10.50% of the variation, respectively, in the sets with contrasting disease susceptibility. Together with the TA59 and TR19 markers, these SNPs can be used in a chickpea breeding scheme to develop wilt resistance.