Pomegranate (Punica granatum L.) cultivation is increasingly threatened by bacterial blight caused by Xanthomonas axonopodis pv. punicae (Xap), highlighting the need for resistant cultivars. This study aimed to identify bacterial-blight-resistant sources from indigenous wild Daru populations and assess their potential through hybridization. Wild Daru germplasm was surveyed, collected, and screened using artificial challenge inoculation, with attached leaf assays providing insights into resistance under more realistic conditions. This study identified genotypes SH-14 and SH-16 as having the lowest disease severity (13.30%) and longest incubation periods (9.50 days). SSR marker analysis of 20 primers across 23 genotypes revealed 1119 scorable bands with a high polymorphism ratio of 92.58%. Phylogenetic analysis and clustering highlighted significant genetic diversity and unique alleles in resistant wild genotypes. Hybridization studies with commercial cultivars showed the Bhagwa × SH-16 cross achieving the highest fruit set (88.90%), while the Kandhari Kabuli × SL-23 cross had the lowest (11.0%). Fruit retention varied, with Bhagwa × SL-23 and Kandhari Kabuli × SR-11 having the highest retention percentages. These findings underscore the potential of Himalayan wild germplasm in developing bacterial-blight-resistant pomegranates and emphasize the integration of molecular markers and hybridization in breeding efforts. The research also provides valuable insights for the development of new pomegranate cultivars with enhanced resistance and improved yield potential. Future research will focus on evaluating hybrid progenies, constructing genetic linkage maps, and identifying specific genes associated with bacterial blight resistance in pomegranate.