This study examines how intraspecific competition influences the shift in oviposition timing of Philornis downsi, an invasive parasitic fly threatening Galapagos land bird species, particularly endemic Darwin’s finches. Historically classified as an obligate nestling parasite, P. downsi is now observed ovipositing during host incubation. The research identifies intraspecific competition, driven by host density and infestation patterns, as a key factor in this shift. A comparison with data from the ancestral population of P. downsi in mainland Ecuador, where oviposition during incubation was not observed, suggests that increased competition in the Galápagos drives earlier oviposition. This shift helps the parasite mitigate larval crowding and resource depletion, though it likely comes with potential trade-offs. These findings have important implications for understanding early stage host-parasite dynamics in isolated ecosystems and the conservation of endangered Darwin’s finches. This file contains the 2012-2024 long-term dataset.