Escherichia coli O157:H7 is a potentially fatal foodborne pathogen with a putative reservoir for human infection in feedlot cattle. In order to more effectively identify targets for intervention strategies, we aimed in this study to (1) assess the role of various feedlot habitats in E. coli O157:H7 propagation and (2) provide a framework for examining the relative contributions of animals and the surrounding environment to observed pathogen dynamics. To meet these goals, we developed a mathematical model to track bacterial population dynamics inside and outside the host. We used E. coli O157:H7 microbiological and epidemiological literature to characterize E. coli O157:H7 habitats at the pen level and account for E. coli O157:H7 population processes in water troughs, feedbunks, cattle hosts, and pen floors in the model. Simulations indicated that E. coli O157:H7 was capable of maintaining viable populations in the feedlot without net growth in the cattle gastrointestinal tract, suggesting E. coli O157:H7 may not always act as an obligate parasite. Water troughs and contaminated pen floors appeared to be particularly influential sources driving E. coli O157:H7 population dynamics and thus would serve as prime environmental targets for interventions to effectively reduce the E. coli O157:H7 load at the pen level.