AbstractPathogens utilize different modes of transmission to maximize transmission success. In vector‐borne disease systems, both vertical and horizontal modes of transmission are common, but the relative contribution of these modes is not well understood but may be determined by host genetics, physiology, or environmental conditions. This study focuses on an emerging tick‐borne relapsing fever pathogen, Borrelia miyamotoi, that can be transmitted both vertically and horizontally. The enzootic cycle of this pathogen has not been described in the western USA where it was recently found in the tick species, Ixodes pacificus. Our field surveys found that all three life stages of I. pacificus carry the pathogen, and therefore, all stages pose some level of disease risk to humans. The prevalence of infection increases with each life stage suggesting that horizontal transmission is important in the persistence of this pathogen in the enzootic cycle. In support of this finding, we found that small mammal hosts that are frequently parasitized by juvenile stages of I. pacificus were infected with B. miyamotoi and may therefore function as a source of horizontal transmission and enzootic maintenance of this disease. Our data show that in the western USA B. miyamotoi is maintained in natural populations by both transovarial transmission and transmission from blood meal hosts and that synchronous phenology of juvenile stages of I. pacificus may facilitate the transmission dynamics of B. miyamotoi and other vertically transmitted, vector‐borne pathogens.