Colter studied at the California School of Design in San Francisco and apprenticed in an architect's office there, then taught drawing in St Paul for fifteen years before the Fred Harvey Company took her on. From 1910 until she retired in 1948 she was its chief architect and decorator, designing the hotels, lodges and rest houses that the company ran along the Atchison, Topeka and Santa Fe Railway. She worked by research rather than by style: months of fieldwork among Ancestral Puebloan ruins, Hopi villages and Spanish mission churches preceded each design, and she specified local stone and had masons lay it to match the strata it came from. Her buildings were invented histories, complete with fictional biographies for their imagined builders, and they set the pattern for what became National Park Service rustic architecture. Four of her Grand Canyon buildings were made a National Historic Landmark in 1987.