To better understand the ecology and evolutionary dynamics of Vibrio cholerae strains circulating in a cholera endemic region, we sequenced 757 genomes from human clinical and environmental sources, spanning past and recent cholera outbreaks over a period of nearly two decades, the largest study of its kind. In doing so we show that V. cholerae is endemic to the freshwater environment in and around northern India.  Notably, disease occurs seasonally, particularly in the so-called "hotspot" communities lacking access to clean drinking water and effective sanitation. Our data show bacterial population decline and the persistence of multiple sub-lineages of the globally successful epidemic 7PET (the seventh pandemic El Tor) lineage that circulated in humans across northern India during this time. Additionally, we reveal the different evolutionary dynamics of 7PET and non-7PET V. cholerae circulating in the environment and in symptomatic or asymptomatic disease. By focusing on isolates linked to declared outbreaks in the region, we dissect outbreak dynamics in detail and report co-isolation of non-7PET strains thriving in freshwater ecosystems. Overall, our study sheds light into the concurrent roles that diverse lineages of V. cholerae coexisting in a region play in human disease. This not only reveals important biology that will help us predict the emergence of future lineages with epidemic potential but also has significant implications for health initiatives aiming to reduce cholera burden in cholera endemic settings.