Borrelia burgdorferi(Bb) andBabesia microti(Bm) are vector-borne zoonotic pathogens commonly found co-circulating inIxodes scapularisandPeromyscus leucopuspopulations. The restricted distribution and lower prevalence ofBmhas been historically attributed to lower host-to-tick transmission efficiency and limited host ranges. We hypothesized that prevalence patterns are driven by coinfection dynamics and vertical transmission. We use a multi-year, multiple location, longitudinal dataset with mathematical modelling to elucidate coinfection dynamics betweenBbandBmin natural populations ofP. leucopus, the most competent reservoir host for both pathogens in the eastern USA. Our analyses indicate that, in the absence of vertical transmission,Bbis viable at lower tick numbers thanBm.However, with vertical transmission,Bmis viable at lower tick numbers thanBb. Vertical transmission has a particularly strong effect onBmprevalence early in the active season while coinfection has an increasing role during the nymphal peak. Our analyses indicate that coinfection processes, such as facilitation ofBminfection byBb, have relatively little influence on the persistence of either parasite. We suggest future work examines the sensitivity ofBmvertical transmission and other key processes to local environmental conditions to inform surveillance and control of tick-borne pathogens.