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Cholera, a disease of antiquity, is still festering in developing countries that lack safe drinking water and sewage disposal. <i>Vibrio cholerae</i>, the causative agent of cholera, has developed multi-drug resistance to many antimicrobial agents. In aquatic habitats, phages are known to influence the occurrence and dispersion of pathogenic <i>V. cholerae</i>. We isolated <i>Vibrio</i> phage VMJ710 from a community sewage water sample of Manimajra, Chandigarh, in 2015 during an outbreak of cholera. It lysed 46% of multidrug-resistant <i>V. cholerae</i> O1 strains. It had significantly reduced the bacterial density within the first 4–6 h of treatment at the three multiplicity of infection (MOI 0.01, 0.1, and 1.0) values used. No bacterial resistance was observed against phage VMJ710 for 20 h in the time–kill assay. It is nearest to an ICP1 phage, i.e., <i>Vibrio</i> phage ICP1_2012 (MH310936.1), belonging to the class <i>Caudoviricetes</i>. ICP1 phages have been the dominant bacteriophages found in cholera patients’ stools since 2001. Comparative genome analysis of phage VMJ710 and related phages indicated a high level of genetic conservation. The phage was stable over a wide range of temperatures and pH, which will be an advantage for applications in different environmental settings. The phage VMJ710 showed a reduction in biofilm mass growth, bacterial dispersal, and a clear disruption of bacterial biofilm structure. We further tested the phage VMJ710 for its potential therapeutic and prophylactic properties using infant BALB/c mice. Bacterial counts were reduced significantly when phages were administered before and after the challenge of orogastric inoculation with <i>V. cholerae</i> serotype O1. A comprehensive whole genome study revealed no indication of lysogenic genes, genes associated with possible virulence factors, or antibiotic resistance. Based on all these properties, phage VMJ710 can be a suitable candidate for oral phage administration and could be a viable method of combatting cholera infection caused by MDR <i>V. cholerae</i> pathogenic strains.