Telomere lengths and telomere dynamics can correlate with lifespan, behaviour and individual quality. Such relationships have spurred interest in understanding variation in telomere lengths and their dynamics within and between populations. Many studies have identified how environmental processes can influence telomere dynamics, but the role of genetic variation is much less well characterized. To provide a novel perspective on how telomeric variation relates to genetic variability, we longitudinally sampled individuals across a narrow hybrid zone (n = 127 samples), wherein two Manacus species characterized by contrasting genome‐wide heterozygosity interbreed. We measured individual (n = 66) and population (n = 3) differences in genome‐wide heterozygosity and, among hybrids, amount of genetic admixture using RADseq‐generated SNPs. We tested for population differences in telomere lengths and telomere dynamics. We then examined how telomere lengths and telomere dynamics covaried with genome‐wide heterozygosity within populations. Hybrid individuals exhibited longer telomeres, on average, than individuals sampled in the adjacent parental populations. No population differences in telomere dynamics were observed. Within the parental population characterized by relatively low heterozygosity, higher genome‐wide heterozygosity was associated with shorter telomeres and higher rates of telomere shortening—a pattern that was less apparent in the other populations. All of these relationships were independent of sex, despite the contrasting life histories of male and female manakins. Our study highlights how population comparisons can reveal interrelationships between genetic variation and telomeres, and how naturally occurring hybridization and genome‐wide heterozygosity can relate to telomere lengths and telomere dynamics.