Mammalian genomes are packaged into a specifically tailored chromatin structure, the regulation of which depends on several superimposed layers of organization that includes the chemical modifications of the DNA, epigenetic modifications of the nucleosomes and the high-order organisation of chromatin compartments inside the nucleus. Yet, the impact of genome reshuffling on this 3D organization during gametogenesis remains unclear. Here, we take advantage of chromosome conformation capture followed by deep sequencing (Hi-C) in combination with SNP genotyping and cytological analysis of crossover events to study how genome folding and recombination landscapes are affected by large-scale genome reshuffling in the germ line. To this aim we analyzed a unique wild population of house mice characterized by a recent evolutionary origin and the presence of chromosomal fusions. The experimental procedures in the germ line were preceded by the isolation of enriched germ cell populations attained by fluorescent-activated cell sorting. Our results show that chromosomal fusions alter the nuclear architecture during meiosis at different hierarchy levels, causing a profound impact on the inter- and intra-chromosomal interactions ratio in the germline. We detected an increase rate of heterologous interactions in primary spermatocytes, affecting both the length of chromosome axes and chromatin loops. Overall, our results provide new insights into how genome reshuffling influences chromatin folding and nuclear architecture, especially in the context of the dramatic chromatin changes that take place during the formation of the germ line.