Ticks are obligate hematophagous arthropods, but may have to endure extended time (1-2years) between feedings. During these off-host periods, ticks must contend with a multitude of environmental stresses including prolonged or repeated exposure to desiccating conditions. In this study, we measured the energetic consequences of single and repeated bouts of dehydration of American dog ticks, Dermacentor variabilis, and examined the impact of energy reserves on tick survival during dehydration. Recently molted ticks exposed to a single period at 0% relative humidity (RH) for 5d lost ∼26% of their body water and showed 1.3- and 1.7-fold reductions in protein and lipid, respectively. These reduced energy reserves coincided with increased O2 consumption in dehydrated ticks. Exposure to repeated cycles of dehydration (0% RH, 48h) and rehydration (100% RH, 24h) also reduced energy reserves; however, ticks were able to fully recover their body water after 12 cycles of dehydration/rehydration and endured >20 cycles. Starvation of ticks, in the absence of dehydration, for 18 or 36weeks resulted in the loss of ∼20-40% of protein and 60% of lipid reserves. When ticks were exposed to continuous dehydration at 0% RH, their survival after 18weeks of starvation was only minimally impacted; however, individuals starved for 36weeks succumbed to dehydration much more rapidly than recently fed ticks. Both single and repeated dehydration exposures resulted in substantial energetic costs and ticks with limited energy reserves were more susceptible to dehydration-induced mortality, indicating that adequate energy reserves are critical for tolerance to dehydration stress and long-term success of ticks.