Recent studies have shown that sensory stimulation can optimize memory consolidation in the sleeping brain for simple lab-based tasks. Based on these earlier results, we developed a closed-loop auditory stimulation (CLAS) system to more precisely target sensory stimulation and test whether this method can improve the more complex skill of spatial navigation in an urban environment. Forty participants (Mean age = 26.2 years, F = 18) were trained to navigate within a large and detailed urban environment in virtual reality. Participants first learned the environment by freely navigating to specific points of interest (24 unique landmarks) in a virtual city. As participants navigated, they encountered different auditory cues (e.g., the barking of a dog near a park) associated with areas in the environment. Following learning, all participants underwent a 90-min polysomnographically-recorded nap, with half the participants receiving CLAS. CLAS detects slow oscillations during non-rapid eye movement (NREM) sleep using a minimum negative threshold criterion coupled with online automated sleep staging, to trigger delivery of short (700 ms) auditory cues during the down-state to up-state transition (DUPT). After sleeping, participants were tested in 6 of the previously trained routes. Compared with controls, the CLAS treated group was significantly faster in post-nap navigation (p<0.01). Additionally, CLAS participants showed an increase in DUPT phase-locked spindle activity in both the slow (9–12 Hz) and fast (12–16 Hz) frequency bands. No effect of the CLAS on sleep architecture was observed. CLAS successfully improves the complex task of navigation in a virtual environment without any negative effects on sleep architecture. This work was supported by DARPA award W911NF-16-2-007. Disclaimer: The views, opinions and/or findings expressed are those of the author and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government.