Telomere length and shortening rate are increasingly used as biomarkers for long-term costs in ecological and evolutionary studies because of their relationships with survival and fitness. Telomere length can be heritable, but both early-life conditions and later-life stressors can create variation in telomere shortening rate. Studies on between-population telomere length and dynamics are mostly lacking, despite the expectation that populations exposed to varying environmental constraints would present divergent telomere length patterns. Pied flycatcher (Ficedula hypoleuca) is a passerine bird spending the non-breeding period in sub-Saharan Africa but breeding across Eurasia (from Spain to western Siberia). Populations show marked differences in migration distance, genetics, breeding parameters, and egg components. We studied the large-scale variation of telomere length, early-life dynamics and heritability in the pied flycatcher by comparing six European populations across a north-south gradient (Finland, Estonia, England and Spain). There were clear population differences in telomere length, with English birds having the longest telomeres, followed by Spanish and lastly by Estonian and Finnish birds. Early-life telomere shortening rate tended to vary between populations, and faster nestling growth affected telomeres more negatively in northern than southern populations. The heritability of telomere length was moderate (h2 = 0.34 - 0.40), with stronger heritability to paternal than maternal telomere length. There was also evidence indicating that the level of paternal heritability could differ between populations. While the sources of between-population differences in telomere-related biology remain to be identified (i.e. genetics, environmental factors), our study illustrates the need to expand telomere studies at the between-population level.