It was first settled as the present-day city in 1876, when Thomas F. McMillan built a cabin just north of what is now main town. The name Flagstaff comes from an actual flagpole made from a stripped pine tree that was erected on July 4, 1876, at Antelope Spring, which McMillan was using as his sheep camp.

Fifty thousand years ago, a giant fireball streaked across the North American sky. The meteorite weighed 300,000 tons and traveled at a speed of 26,000 miles per hour (12 kilometers per second). When it struck the earth approximately 37 miles east of what is now Flagstaff and 18 miles west of Winslow in the northern Arizona desert, it exploded with the force of 2½ million tons of TNT, or about 150 times the force of the atomic bomb that destroyed Hiroshima. When the dust settled, what remained was a crater three-quarters of a mile (about 1 kilometer) wide and 750 feet deep. Formerly known as the Canyon Diablo Crater, it has since been renamed the Barringer Crater in honor of Daniel Barringer, who first recognized that it was produced by a meteorite impact.

Flagstaff takes one of its nicknames from its legislative designation as the world's first International Dark Sky City, a deliberate dark sky preserve area with measures to reduce light pollution. This was one of the world's first coordinated legislative efforts to do so, and is generally regarded as a world precedent in dark sky preservation.

Flagstaff became a popular tourist stop along Route 66 after its construction in 1926. In early September, the city hosts an annual event, Route 66 Days, to highlight its connection to the famous highway.

The city sits in middle of the largest ponderosa pine forest in the country, and the trees give off an aromatic scent that makes the entire city smell like a vanilla-scented paradise.

Though one of the least-sunny cities in Arizona, Flagstaff still ranks among the United States' sunniest cities, having sunshine for an average 78% of the year. And with an average of 100.6 inches of snow per year, it's also one of the snowiest in the nation.

The Sinagua were a pre-Columbian culture that occupied a large area in central Arizona from the Little Colorado River, near Flagstaff, to the Verde River, near Sedona, between approximately 500 CE and 1425 CE. Since fully developed Sinagua sites emerged in central Arizona around 650 CE, it is believed they migrated from east-central Arizona, possibly emerging from the Mogollon culture.

In 1906, Percival Lowell--a wealthy Bostonian who had founded Lowell Observatory in Flagstaff, Arizona, in 1894--started an extensive project in search of a possible ninth planet, which he termed "Planet X". On February 18, 1930, 23-year-old Clyde Tombaugh discovered a moving object on photographic plates taken on January 23 and 29. Each member of the Lowell Observatory was allowed to vote on a short-list of three potential names: Minerva (which was already the name for an asteroid), Cronus (which had lost reputation through being proposed by the unpopular astronomer Thomas Jefferson Jackson See), and Pluto. Pluto received a unanimous vote. In 2006, the International Astronomical Union reclassified Pluto as a dwarf planet.

The many settlement sites scattered throughout the Wupatki National Monument were built by the Ancient Pueblo People, more specifically the Cohonina, Kayenta Anasazi, and Sinagua. Wupatki, which means "Tall House" in the Hopi language, was first inhabited around 500 AD. It is a multistory Sinagua pueblo dwelling comprising over 100 rooms and a community room and the northernmost ballcourt ever discovered in North America. Although Wupatki appears empty and abandoned today, it is remembered and cared for. Stories of Wupatki are passed on among Hopi, Navajo, Zuni, and other Native American tribes in the region, who believe that the people who lived and died here remain as spiritual guardians.

According to Travel and Leisure, the Hotel Monte Vista, which once played host to big-name celebrities, is now the most haunted spot in Arizona. Numerous hauntings have been reported, including a phantom bellboy who knocks on doors and announces "room service," then disappears when guests open the door. Legendary actor John Wayne claimed to have seen the ghostly figure of a bellboy standing outside of room 210. Mr. Wayne reported that the ghost seemed friendly and that he did not feel threatened by its presence.