Aging of the follicular environment negatively impacts oocyte quality and developmental potential. This study demonstrates that young follicular environments can rejuvenate aged oocytes by improving their maturation, blastocyst formation, and live birth rates. By transplanting oocytes into young follicles, the study shows that aged oocytes exhibit enhanced interaction with somatic cells, a more youthful transcriptome, remodeled metabolome, improved mitochondrial function, and better meiotic chromosome segregation. These findings suggest that a follicular somatic cell-based therapy could treat age-associated female infertility. Oocyte quality declines with age due to reduced somatic cell function, including decreased proliferative activity, increased DNA damage, and impaired mitochondrial function. A 3D ex vivo culture system was developed to study the effects of follicular aging on oocyte quality. Transplanting young oocytes into aged follicles resulted in reduced meiotic maturation and developmental potential, while young oocytes in aged follicles showed improved maturation and blastocyst formation. Conversely, aged oocytes in young follicles exhibited enhanced developmental competence. The study also found that young follicular environments enhance the formation of transzonal projections (TZPs), which are critical for nutrient and metabolic exchange between granulosa cells and oocytes. This improved communication led to metabolic and transcriptomic remodeling of aged oocytes, as well as enhanced mitochondrial function and reduced oxidative stress. Additionally, young follicular environments improved meiotic chromosome segregation, reducing the incidence of aneuploidy and chromosomal abnormalities. The findings suggest that the young follicular environment can partially restore the quality and developmental competence of aged oocytes. However, complete rejuvenation is not achieved, as blastocyst formation and live birth rates remain lower than those in young oocytes. The study highlights the importance of follicular somatic cells in maintaining oocyte quality and suggests that future therapies could focus on restoring the follicular environment to improve oocyte quality and fertility in aging women.Aging of the follicular environment negatively impacts oocyte quality and developmental potential. This study demonstrates that young follicular environments can rejuvenate aged oocytes by improving their maturation, blastocyst formation, and live birth rates. By transplanting oocytes into young follicles, the study shows that aged oocytes exhibit enhanced interaction with somatic cells, a more youthful transcriptome, remodeled metabolome, improved mitochondrial function, and better meiotic chromosome segregation. These findings suggest that a follicular somatic cell-based therapy could treat age-associated female infertility. Oocyte quality declines with age due to reduced somatic cell function, including decreased proliferative activity, increased DNA damage, and impaired mitochondrial function. A 3D ex vivo culture system was developed to study the effects of follicular aging on oocyte quality. Transplanting young oocytes into aged follicles resulted in reduced meiotic maturation and developmental potential, while young oocytes in aged follicles showed improved maturation and blastocyst formation. Conversely, aged oocytes in young follicles exhibited enhanced developmental competence. The study also found that young follicular environments enhance the formation of transzonal projections (TZPs), which are critical for nutrient and metabolic exchange between granulosa cells and oocytes. This improved communication led to metabolic and transcriptomic remodeling of aged oocytes, as well as enhanced mitochondrial function and reduced oxidative stress. Additionally, young follicular environments improved meiotic chromosome segregation, reducing the incidence of aneuploidy and chromosomal abnormalities. The findings suggest that the young follicular environment can partially restore the quality and developmental competence of aged oocytes. However, complete rejuvenation is not achieved, as blastocyst formation and live birth rates remain lower than those in young oocytes. The study highlights the importance of follicular somatic cells in maintaining oocyte quality and suggests that future therapies could focus on restoring the follicular environment to improve oocyte quality and fertility in aging women.