Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere dynamics driven by thermal stress are of particular interest during the early post-natal stages of altricial birds because nestlings quickly shift from being ectothermic to poikilothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but investigations within species that transition from ectothermy to endothermy are lacking. Also, ambient temperature influences parental brooding behavior, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves, and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that correspond to three different thermoregulatory stages (ectothermic, poikilothermic and endothermic respectively); we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (poikilothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at five days old) compared to controls. Lower brooding effort was associated with shorter telomeres in 12 day old nestlings. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behavior during growth.