Urban habitats can shape interactions between hosts and parasites by altering within-host processes such as resistance. Artificial light at night is common in urban environments, and chronic exposure can impair host immunity in ways that may increase infection. However, studies of causal links between this stressor, immunity, and infection dynamics are rare, particularly in migratory animals. Here, we experimentally tested how artificial light at night affects cellular immunity and intensity of infection with haemosporidian parasites across the annual cycle of migrant and resident subspecies of the dark-eyed junco (Junco hyemalis). We exposed an experimental group to light at night and compared them to control birds under nighttime darkness. Both groups were monitored as they passed through short days simulating early spring to longer days simulating the breeding season, followed by fall migration. Using generalized additive models, we show that artificial light at night increased inflammation, and leukocyte counts were greatest in early spring and fall. At the beginning of the experiment, few birds had active infections based on microscopy, but nested PCR revealed that many birds had chronic infections. Artificial light at night increased parasitemia across the annual cycle, with pronounced peaks in spring and fall that were largely absent in control birds. Because all birds were kept in indoor aviaries to prevent vector exposure, these pulses in parasite intensity indicate relapse of chronic infection during costly life history stages (i.e., reproduction, migration). Although the immunological and parasitological time series were in phase for control birds, cross-correlation analyses revealed that artificial light at night desynchronized leukocyte profiles and haemosporidian intensity, which could suggest immune dysregulation. Our study shows how a common anthropogenic influence can shape within-host processes to affect infection dynamics.