Following synaptic activation, excitatory neurotransmitter glutamate released to synapses must be removed by glutamate transporters to terminate the signal and to protect neurons from excitotoxicity. Although neurons also contribute, most of the released glutamate is taken up by astrocytes. For this purpose, astrocytes extend thousands of thin cellular processes to surround synapses within neuronal networks. The mechanisms underlying the localization of glutamate transporters within these finely branched processes, however, are not known. In this study, we found that the trimeric transmembrane transporter domain of glutamate transporters localizes to the tips of filopodia, even after deletion of their N- and C-terminal cytoplasmic tails, which contain binding sites for cellular proteins. Furthermore, the trimeric transporter domain of the neutral amino acid transporter ASCT1 also localized to the filopodia tips, suggesting that filopodia tip localization is a property common to trimeric transporters. Neither transporter activity nor astrocyte-specific proteins are required for filopodia tip localization. We also found that transporter cores localized to filopodia tips strengthen the attachment of the filopodia to external substrates, thereby stabilizing the filopodia. The trimeric core domains of glutamate transporters also localized to finely branched astrocyte processes, analogous to filopodia, in organotypic hippocampal slice cultures. Together, our results demonstrate that, in addition to glutamate uptake, glutamate transporters play a structural role in promoting the stabilization of astrocyte fine processes.