Heartwater is a tick-borne disease (TBD) of wild and livestock ruminants that threatens food security and the economy throughout much of Africa. Furthermore, the geographic range of heartwater is expanding and is predicted to continue doing so. Despite this, our understanding of heartwater dynamics lags far behind that of many other TBDs. We are therefore limited in our ability to design effective disease control strategies. In this study, we derive and analyse a mathematical model of heartwater dynamics. We analyse our model to predict the most influential parameters for disease risk, both in terms of new outbreaks and in heartwater-endemic regions. We show that the host-finding efficiency of ticks is the most influential parameter affecting outbreak risk. Also, outbreak risk is highly sensitive to the impact of the heartwater pathogen on tick fitness – a previously unexplored concept for any TBD system. In areas where heartwater is established, we show that disease can be controlled via enzootic stability (prolonged host immunity attained via frequent pathogen exposure). However, the maintenance of enzootic stability was dependent on several ecological and physiological parameters. Regarding practical output, we suggest prioritizing tick control measures during periods when ticks are most active in terms of dispersing towards hosts, so as to mitigate heightened outbreak risk. In addition, given the specificity of conditions required for enzootic stability, we caution against relying solely on enzootic stability for long-term heartwater protection. More broadly, our study highlights important tick life history parameters that have been neglected by previous TBD models.