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Pomegranate bacterial blight caused by <i>Xanthomonas axonopodis</i> pv. <i>punicae</i> (<i>Xap</i>) is a highly destructive disease. In the absence of host resistance to the disease, we aimed to evaluate the biocontrol potential of endophytic bacteria against <i>Xap</i>. Thus, in this study, we isolated endophytes from pomegranate plants, identified them on the basis of 16S rDNA sequencing, tested them against <i>Xap</i>, and estimated the endophyte-mediated host defense response. The population of isolated endophytes ranged from 3 × 10⁶ to 8 × 10⁷ CFU/g tissue. Furthermore, 26 isolates were evaluated for their biocontrol activity against <i>Xap</i>, and all the tested isolates significantly reduced the in vitro growth of <i>Xap</i> (15.65% ± 1.25% to 56.35% ± 2.66%) as compared to control. These isolates could reduce fuscan, an uncharacterized factor of <i>Xap</i> involved in its aggressiveness. Lower blight incidence (11.6%) and severity (6.1%) were recorded in plants sprayed with endophytes 8 days ahead of <i>Xap</i> spray (Set-III) as compared to control plants which were not exposed to endophytes (77.33 and 50%, respectively%) during in vivo evaluation. Moreover, significantly high phenolic and chlorophyll contents were estimated in endophyte-treated plants as compared to control. The promising isolates mostly belonged to the genera <i>Bacillus</i>, <i>Burkholderia</i>, and <i>Lysinibacillus</i>, and they were deposited to the National Agriculturally Important Microbial Culture Collection, India.