Ixodes scapularis is the principal tick vector of the Lyme borreliosis agent Borrelia burgdorferi and other tick-borne zoonoses in northeastern North America. The degree of seasonal synchrony of nymphal and larval ticks may be important in influencing the basic reproductive number of the pathogens transmitted by I. scapularis. Because the seasonal phenology of tick vectors is partly controlled by ambient temperature, climate and climate change could shape the population biology of tick-borne pathogens. We used projected monthly normal temperatures, obtained from the second version of the Canadian Coupled Global Climate Model (CGCM2) under emissions scenario A2 of the Intergovernmental Panel on Climate Change for a site in southern Ontario, Canada, to simulate the phenology of I. scapularis in a mathematical model. The simulated seasonal abundance of ticks then determined transmission of three candidate pathogens amongst a population of white-footed mice (Peromyscus leucopus) using a susceptible-infected-recovered (SIR) model. Fitness of the different pathogens, in terms of resilience to changes in tick and rodent mortality, minima for infection duration, transmission efficiency and particularly any additional mortality of rodents specifically associated with infection, varied according to the seasonal pattern of immature tick activity, which was different under the temperature conditions projected for the 2020s, 2050s and 2080s. In each case, pathogens that were long-lived, highly transmissible and had little impact on rodent mortality rates were the fittest. However, under the seasonal tick activity patterns projected for the 2020s and 2050s, the fitness of pathogens that are shorter-lived, less efficiently transmitted, and more pathogenic to their natural hosts, increased. Therefore, climate change may affect the frequency and distribution of I. scapularis-borne pathogens and alter their evolutionary trajectories.