Fluorescent drug conjugates enable the selective visualization of proteins in cell models, primary cultures, and tissue preparations. These compounds have become valuable tools in neuroscience in investigating the expression and function of ion channels, receptors, and transporters. In this project, we explored the utility of fluorescent drug conjugates in visualizing the serotonin transporter (SERT) in the brain. We made use of a recently developed class of fluorescent compounds called PyrAtes which offer interesting chemical properties, photostability, and large Stokes shifts. Herein, two compounds were designed and synthesized each with a PyrAte fluorophore attached to (S)-citalopram, a selective serotonin reuptake inhibitor (SSRI), via either a six-carbon chain linker (PYR-C6-CIT) or a three-carbon chain linker (PYR-C3-CIT). The activity of these resulting compounds was observed in HEK293 cells overexpressing SERT using cell-based radioligand uptake assays, electrophysiology, and confocal microscopy experiments. Additionally, imaging endogenously expressed SERT was explored ex vivo in acute mouse brain slices using two-photon microscopy. Both compounds were found effective and specific in the fluorescent labelling of SERT. We have shown for the first time a fluorescent (S)-citalopram conjugate that binds specifically to endogenously expressed SERT. Our results not only confirm the utility of such compounds in the fluorescence imaging of transporters, but also provide some insights into ways of improving the design of PyrAte fluorophores and their fluorescent drug conjugates in the future.