Three-dimensional genome organization in the cell nucleus reflects its functional state and is one of the regulatory levels of gene expression. Thus, the extensive exploration of the relationship between the spatial organization of the genome and its functioning is very important. In this work, the three-dimensional genome organization in growing oocytes of Galliform birds was analyzed in detail. Avian oocytes have giant transcriptionally active nuclei that are distinct from somatic interphase nuclei in their almost complete lack of structural constraints on chromosome decondensation. The radial distribution of three groups of chromosomes with different sizes and gene densities in the nuclei of chicken and Japanese quail oocytes was analyzed by confocal laser scanning microscopy followed by 3D reconstruction. The chromosome position relative to the nuclear center was estimated by analyzing its localization in certain radial nuclear zones and directly measuring the distance from the nuclear center to the terminal regions and center of chromosome gravity. It was shown that, in transcriptionally active nuclei of avian oocytes, chromosomes are localized at a significant distance from the nuclear envelope; gene-rich microchromosomes are localized mainly on the periphery of the region occupied by the whole chromosome set, rather than in the nuclear center. Therefore, the radial distribution of lampbrush chromosomes in oocyte nuclei differs from the ordered spatial arrangement of chromosomes in the interphase nucleus with gene-rich chromosome territories being located at the nuclear center and gene-poor territories positioned at the nuclear periphery. By visualizing 3D-preserved lampbrush chromosomes in the intact nucleus, we confirmed the presence of repulsion forces between lateral loops of lampbrush half-bivalents and the lack of interactions between heterochromatic segments of different bivalents at the lampbrush stage of oogenesis.