The nuclear pore complexes (NPCs) are channels primarily responsible for nucleocytoplasmic exchanges in eukaryotic cells. Growing evidence indicates that they also play a role in chromatin stability, DNA repair as well as transcriptional regulation. Many inducible genes such as GAL1 relocate to the NPC upon activation suggesting that pores may coordinate transcription and mRNA export. The Ulp1 SUMO protease is anchored to the NPC through Mlp1/2 and Nup60. Ulp1 can be delocalized from the periphery by deleting the N-terminal NPC targeting domain, NUP60 or MLP1 and MLP2. Release of Ulp1 from the NPC positively affects GAL1 transcription derepression but has no effect on activation kinetics. The increase of GAL1 mRNA is accompanied by a loss of Ssn6 sumoylation. Moreover, the release of Ulp1 from its location at the NPC and loss of Ssn6 sumoylation also result in upregulated HXK1 mRNA levels. Here we show that Ulp1 is located at the NPC in the presence of glucose and galactose. Furthermore, absence of Ulp1 at the NPC induces a dominant effect on GAL1 gene expression and does not affect GAL1 mRNA stability. Consistent with our model, loss of sumoylation of Gcn5, a histone acetyl transferase component of the SAGA coactivator complex, correlates with increased in GAL1 mRNA levels when cells are shifted from glucose to galactose and increased HXK1 mRNA levels even in the presence of glucose. Moreover, deletion of Cti6, a PHD domain protein that mediates the interaction between Ssn6 and Gcn5, prevents all of our strains from reaching optimal GAL1 gene expression. Finally, increased GAL1 derepression kinetics due to the delocalization of Ulp1 correlates with increased Gal1 protein production suggesting that transcription at the nuclear pore is not essential for correct GAL1 mRNA export and translation in the cytoplasm. Taken together our results suggest a model in which the SUMO protease Ulp1 participates in a general regulation mechanism that controls the desumoylation of proteins bound to genes that relocate to the NPC when activated, ensuring optimal control of gene expression.