During meiotic prophase I, homologous chromosomes pair, synapse and recombine in a tightly regulated process that ensures the generation of genetically variable haploid gametes. Although the mechanisms underlying meiotic cell division have been well studied in model species, our understanding of the dynamics of meiotic prophase I in non-traditional model mammals remains in its infancy. Here, we reveal key meiotic features in previously uncharacterised marsupial species (the tammar wallaby and the fat-tailed dunnart), plus the fat-tailed mouse opossum, with a focus on sex chromosome pairing strategies, recombination and meiotic telomere homeostasis. We uncovered differences between phylogroups with important functional and evolutionary implications. First, sex chromosomes, which lack a pseudo-autosomal region in marsupials, had species specific pairing and silencing strategies, with implications for sex chromosome evolution. Second, we detected two waves of γH2AX accumulation during prophase I. The first wave was accompanied by low γH2AX levels on autosomes, which correlated with the low recombination rates that distinguish marsupials from eutherian mammals. In the second wave, γH2AX was restricted to sex chromosomes in all three species, which correlated with transcription from the X in tammar wallaby. This suggests non-canonical functions of γH2AX on meiotic sex chromosomes. Finally, we uncover evidence for telomere elongation in primary spermatocytes of the fat-tailed dunnart, a unique strategy within mammals. Our results provide new insights into meiotic progression and telomere homeostasis in marsupials, highlighting the importance of capturing the diversity of meiotic strategies within mammals. The generation of haploid gametes is a hallmark of sexual reproduction. And this is accomplished by a complex, albeit tightly regulated, reductional cell division called meiosis. Although meiosis has been extensively studied in eutherian mammal model species, our understanding of the mechanisms regulating chromosome synapsis, recombination and segregation during meiosis progression is still incomplete especially in non-eutherian mammals. To fill this gap and capture the diversity of meiotic strategies among mammals, we study previously uncharacterised representative marsupial species, an evolutionary assemblage that last shared a common ancestry more than 80 million years ago. We uncover novel, hence non-canonical, strategies for sex chromosome pairing, DNA repair, recombination and transcription. Most importantly, we reveal the uniqueness of marsupial meiosis, which includes the unprecedented detection of alternative mechanism (ALT) for the paternal control of telomere length during prophase I. Our findings suggest that ALT (previously only associated to cancer cells) could play a role in telomere homeostasis in mammalian germ cells.