Millions of Lyme disease vector ticks are dispersed annually by songbirds across Canada, but often overlooked as the source of infection. For clarity on vector distribution, we sampled 481 ticks (12 species and 3 undetermined ticks) from 211 songbirds (42 species/subspecies) nationwide. Using PCR, 52 (29.5%) of 176 Ixodes ticks tested were positive for the Lyme disease spirochete, Borrelia burgdorferi s.l. Immature blacklegged ticks, Ixodes scapularis, collected from infested songbirds had a B. burgdorferi infection prevalence of 36% (larvae, 48%; nymphs, 31%). Notably, Ixodes affinis is reported in Canada for the first time and, similarly, Ixodes auritulus for the initial time in the Yukon. Firsts for bird-parasitizing ticks include I. scapularis in Quebec and Saskatchewan. We provide the first records of 3 tick species cofeeding on passerines (song sparrow, Swainson's thrush). New host records reveal I. scapularis on the blackpoll warbler and Nashville warbler. We furnish the following first Canadian reports of B. burgdorferi–positive ticks: I. scapularis on chipping sparrow, house wren, indigo bunting; I. auritulus on Bewick's wren; and I. spinipalpis on a Bewick's wren and song sparrow. First records of B. burgdorferi–infected ticks on songbirds include the following: the rabbit-associated tick, Ixodes dentatus, in western Canada; I. scapularis in Quebec, Saskatchewan, northern New Brunswick, northern Ontario; and Ixodes spinipalpis (collected in British Columbia). The presence of B. burgdorferi in Ixodes larvae suggests reservoir competency in 9 passerines (Bewick's wren, common yellowthroat, dark-eyed junco, Oregon junco, red-winged blackbird, song sparrow, Swainson's thrush, swamp sparrow, and white-throated sparrow). We report transstadial transmission (larva to nymph) of B. burgdorferi in I. auritulus. Data suggest a possible 4-tick, i.e., I. angustus, I. auritulus, I. pacificus, and I. spinipalpis, enzootic cycle of B. burgdorferi on Vancouver Island, British Columbia. Our results suggest that songbirds infested with B. burgdorferi–infected ticks have the potential to start new tick populations endemic for Lyme disease. Because songbirds disperse B. burgdorferi–infected ticks outside their anticipated range, health-care providers are advised that people can contract Lyme disease locally without any history of travel.