Meiosis is a unique cell division in germ cells that is essential for the faithful transmission of hereditary material to the next generation. This dissertation research was undertaken to evaluate the underlying mechanisms of meiotic spindle formation in mammalian oocytes. Stable spindle assembly in oocytes is critical for accurate meiotic division and differs from mitotic cells. Oocytes lack classic centrosomes and instead contain unique acentriolar microtubule organizing centers (aMTOCs) for spindle formation. Our lab developed a novel oocyte-specific Pericentrin (PCNT) knockdown transgenic (Tg) mouse model that lacks functional aMTOCs. Loss of aMTOCs leads highly error-prone meiotic division, aneuploidy and female subfertility. My studies utilized this Tg model to test the function of key aMTOC-associated proteins. The first project demonstrated that CEP215 (Centrosomal Protein 215) is a functional component of oocyte aMTOCs and participates in the regulation of meiotic spindle pole focusing. Moreover, these studies revealed a vital role for AURKA activity in the maintenance of aMTOC organization in oocytes. The second project focused on the role of AURKA, as well as a newly identified liquid-like meiotic spindle domain (LISD) that functions as a dynamic reservoir for microtubule regulatory factors. Our analysis revealed complete loss of pAURKA at spindle poles in PCNT-depleted (Tg) oocytes. Moreover, we showed that LISD assembly depends expressly on aMTOC-associated AURKA. These data support that loss of aMTOC-associated AURKA and failure of LISD assembly contribute to error-prone meiotic division in PCNT-depleted oocytes, underscoring the essential role of aMTOCs for meiotic spindle stability. In addition to aMTOCs, Ran GTPase activity can promote MT nucleation and spindle assembly. Thus, the third study tested Ran function in WT and Tg oocytes. Overexpression of inactive Ran resulted in high rates of chromosome errors in both WT and PCNT-depleted oocytes, supporting its vital role in regulating meiotic spindle stability. Notably, excess Ran activity cannot compensate for the loss of aMTOCs to prevent meiotic errors in Tg oocytes. Taken together these studies support that both Ran and aMTOCs function to regulate meiotic spindle assembly and stability in oocytes.