Telomeres are repetitive DNA sequences that cap the ends of eukaryotic linear chromosomes and play major roles in cell cycle control, cellular lifespan and maintaining genome integrity. Telomere length is an important determinant in health, longevity, and disease, with short telomeres being associated with adverse pathologies. Telomeres naturally shorten with each cell cycle, therefore their length must be regenerated at the outset of each new generation as it is essential for the health span of the offspring. Early embryogenesis is a time of exponential, rapid cell divisions to form a ‘new’ organism, which originates from a single cell. Importantly, telomeres lengthen rapidly during pre-implantation development, and this appears to be a major mechanism by which telomere length is reset across generations; however, there is little understanding of the mechanisms by which this occurs. Thus we conducted a detailed investigation of telomere elongation during mouse pre-implantation embryogenesis. Analysis of mRNA expression of key proteins that regulate telomere elongation (ALT- or telomerase-mediated) showed they were expressed in oocytes and embryos. We developed a highly quantitative qPCR assay which measures telomere length per cell in individual mouse oocytes and embryos. We then conducted an in-depth time course measuring telomere length in oocytes, sperm and across multiple stages of embryogenesis (2-cell, 4-cell, 8-cell, blastocyst), in 4 different crosses involving 2 strains of inbred and 1 strain of outbred mice. We found that telomere elongation occurred during embryogenesis but with subtly different kinetics in each cross. Further, telomere lengths were dynamic in both the Inner Cell Mass and Trophectoderm cell lineages. To investigate whether the capacity for elongation resides within the oocyte itself, we assessed elongation trends in parthenogenetically activated embryos and again found distinct patterns. These results demonstrate that telomere elongation occurs rapidly during embryogenesis, but exhibits distinct patterns dependent on mode of conception.