During Aspergillus nidulans mitosis peripheral nuclear pore complex (NPC) proteins (Nups) disperse from the core NPC structure. Unexpectedly, one predicted peripheral Nup, Gle1, remains at the mitotic NE via an unknown mechanism. Gle1 affinity purification identified MtgA ( M: itotic T: ether for G: le1), which tethers Gle1 to the NE during mitosis, but not during interphase when Gle1 is at NPCs. MtgA is the ortholog of the Schizosaccharomyces pombe telomere-anchoring inner nuclear membrane protein Bqt4. Like Bqt4, MtgA has meiotic roles but is functionally distinct from Bqt4 as MtgA is not required for tethering telomeres to the NE. Domain analyses revealed MtgA targeting to the NE requires its C-terminal transmembrane domain and a nuclear localization signal. Importantly, MtgA functions beyond Gle1 mitotic targeting and meiosis and impacts nuclear and nucleolar architecture when deleted or overexpressed. Deletion of MtgA generates small, round nuclei whereas overexpressing MtgA generates larger nuclei with altered nuclear compartmentalization resulting from NE expansion around the nucleolus. The accumulation of MtgA around the nucleolus promotes a similar accumulation of the endoplasmic reticulum (ER) protein Erg24 lowering its levels in the ER. This study extends the functions of Bqt4-like proteins to include mitotic Gle1 targeting and modulation of nuclear and nucleolar architecture.