During spermatogenesis, genetically variable haploid gametes are generated in a tightly regulated process called meiosis, which includes homologous chromosome pairing, synapsis and recombination. Errors in these processes may lead to aneuploidy and infertility problems. The presence of partially or completely unsynapsed regions induces a transcriptional silencing checkpoint, including the meiotic sex chromosome inactivation (MSCI), to avoid the premature expression of genes that would induce meiotic arrest at pachytene1,2. In marsupials, sex chromosomes lack a pseudo-autosomal region, so the association via a marsupial specific structure called the dense plate (DP) ensures faithful segregation of sex chromosomes in the absence of synapsis and recombination3. Due to their key basal position in the mammalian evolutionary tree, marsupials offer a unique opportunity to explore previously uncharacterized meiotic features, from sex chromosome pairing strategies to X chromosome transcription dynamics. Here, we combine cytological analysis and single-cell RNA sequencing to study the sex chromosome dynamics during meiotic progression in the Australian marsupial tammar wallaby. Our results show that sex chromosomes pair forming the so-called dense plate following different sex chromosome pairing strategies in marsupial species, which correlates with differential sex chromosomes architecture and transcriptional patterns. Remarkably, we detected that the tammar X chromosome is partially transcribed during meiosis and escapes MSCI for much of pachytene, which has important implications for sex chromosome evolution.