Fusarium wilt (FW) of chickpea (Cicer arietinum L.), caused by Fusarium oxysporum f. sp. ciceris (Foc), is a devastating soil-borne disease affecting global chickpea yield and quality. This study investigates the role of microRNAs (miRNAs) and miRNA/target gene interactions in chickpea resistance to FW. Morphological, physiological, biochemical, and molecular analyses were conducted in four chickpea genotypes: WR 315 and Pusa Green 112 (FW-resistant) and JG 62 and ILC 482 (FW-susceptible) at early (2 days post-inoculation) and late (10/12 days post-inoculation) infection stages. Resistant genotypes exhibited strong early defense responses, including enhanced reactive oxygen species (ROS) regulation, salicylic acid induction, and increased proline and protein levels, restricting pathogen proliferation. Susceptible genotypes showed delayed and weaker responses, facilitating disease progression. Based on these findings, small RNA sequencing of stress and control samples from JG 62 and WR 315 at 10 dpi identified 544 miRNAs (406 known, 138 novel), with 50 miRNAs co-localized with Foc resistance QTLs on chromosome 2. A total of 115 miRNAs displayed differential expression, influencing transcription regulation, disease resistance, and metabolism. Poly(A) based qRT-PCR validated 16 miRNAs and their targets, revealing genotype-specific and infection-stage-dependent expression patterns. Notably, Car-miR398 regulated superoxide dismutase activity via copper chaperone targeting. This study provides novel insights into miRNA-mediated resistance mechanisms against FW, facilitating the development of wilt-resistant chickpea varieties.