Single-molecule force spectroscopy (SMFS) is a technique by which a protein is unfolded by the application of force. By analyzing the forces applied to the protein, the configurations the protein adopts during the unfolding process, known as intermediates, are detected. We used atomic force microscopy with modified ultrashort cantilevers, optimized for 1-microsecond resolution, to reexamine the unfolding of the model membrane protein bacteriorhodopsin. Numerous new intermediates were detected, with many separated by as little as two amino acids. Further, the protein unfolding pathways exhibited complex dynamics, including frequent unfolding and refolding, and dwells shorter than 10 µs. By unfolding the proteins from both ends, we revealed complementary sets of intermediates that helped determine the interactions that stabilize these intermediates. These results sharpen the picture of the mechanical unfolding of membrane proteins and suggest that similar dynamics may have been obscured in previous SMFS studies.