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The black-legged tick (<i>Ixodes scapularis</i>) is the primary vector of <i>Borrelia burgdorferi</i>, the causative agent of Lyme disease in North America. However, the prevalence of Lyme borreliosis is clustered around the Northern States of the United States of America. This study utilized a metagenomic sequencing approach to compare the microbial communities residing within <i>Ix. scapularis</i> populations from northern and southern geographic locations in the USA. Using a SparCC network construction model, we performed potential interactions between members of the microbial communities from <i>Borrelia burgdorferi</i>–infected tissues of unfed and blood-fed ticks. A significant difference in bacterial composition and diversity was found between northern and southern tick populations. The network analysis predicted a potential antagonistic interaction between endosymbiont <i>Rickettsia buchneri</i> and <i>Borrelia burgdorferi</i> sensu lato. The network analysis, as expected, predicted significant positive and negative microbial interactions in ticks from these geographic regions, with the genus <i>Rickettsia</i>, <i>Francisella</i>, and <i>Borreliella</i> playing an essential role in the identified clusters. Interactions between <i>Rickettsia buchneri</i> and <i>Borrelia burgdorferi</i> sensu lato need more validation and understanding. Understanding the interplay between the microbiome and tick-borne pathogens within tick vectors may pave the way for new strategies to prevent tick-borne infections.