Telomeres, the protective DNA sequences at chromosome ends, shorten with every cell division. Short telomeres trigger cellular senescence and diminished tissue function. Therefore, telomere length must be regenerated during embryogenesis to ensure viability and health of offspring. While telomere elongation in preimplantation embryos is believed to be largely mediated by the telomerase enzyme complex; exceedingly little is known about this process and its regulation. Characterisation of telomere length in individual mouse oocytes and embryos via qPCR revealed elongation occurs rapidly within the first three cell divisions and again during the morula and blastocyst stages. In parallel, expression of telomere regulatory genes was assessed through an unbiased in silico approach using RNA-seq datasets of mouse, macaque, and human preimplantation embryos. Dynamic patterns of gene expression were observed; in particular, a large cohort of genes was upregulated between the 8-cell and blastocyst, when telomere elongation is maximal. Surprisingly, independent analysis of telomerase genes (Tert, Terc, Dkc1) found decreasing expression with each successive stage of mouse preimplantation development while telomerase activity increased, concurrent with telomere elongation. We next tested the role of oocyte mitochondria in the regulation of this process by measuring telomere elongation in mice with compromised mitochondrial activity, and in response to mitochondrial activators. Ageing or obese mice exhibit embryo oxidative stress, including reduced mitochondria membrane potential and elevated mitochondrial reactive oxygen species (mtROS) production, that is recapitulated by in vivo rotenone (Complex-I inhibitor) exposure. In each of the mitochondria dysfunction models, telomere length was reduced in blastocysts, specifically the inner cell mass (ICM), indicating deficient telomere resetting. Following embryo transfer to surrogates for gestion, shorter telomeres were maintained in fetal tissues, predicting shorter lifespan in offspring. Interestingly, Tert, Terc, and Dck1 expression and telomerase activity were increased in 8-cell embryos in response to rotenone-induced oxidative stress, however expression in the latter stages of development was unaffected. Oocytes from rotenone-exposed, ageing, or obese mice were treated with compounds known to activate oocyte mitochondria (BGP-15, Metformin, MitoQ) to determine if the telomere deficiency is reversible. Remarkably, mitochondria-activating compounds administered prior to fertilisation reduced mtROS production and restored telomere lengths in ICMs to similar levels as those from young/lean controls. Thus, oocyte mitochondrial dysfunction, including from obesity and ageing, leads to impaired embryo telomere resetting, likely contributing to poorer health outcomes, including reduced lifespan. Importantly, the telomere resetting process is modifiable during preimplantation embryogenesis to reverse this developmental defect.