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Agoura Hills is considered the "Gateway to the Santa Monica Mountains National Recreation Area." The city is unofficially divided into a number of varied districts, the most notable of these districts include Downtown, Forest Cove, South End, Malibu Junction, East Agoura, and Old Agoura. Agoura has a Mountain called Negrohead Mountain. Named after John Ballard.

Agoura Hills was first settled by the Chumash Indians, and later by Spanish Franciscan missionaries. In 1845. José Maria Dominguez was given Rancho Las Virgenes as a Mexican land grant and Maria Antonia Machado de Reyes later purchased the rancho from Dominguez in 1845. The "Reyes Adobe" ranch headquarters can still be found today in a museum along Reyes Adobe Rd. in central Agoura Hills. By 1900, Agoura Hills was being used as a popular stage stop for travelers along the Camino Real because of its natural spring at the foothills of Ladyface Mountain, one of Agoura Hills' defining geographic features. In the 1920s, the community was briefly known as Picture City, as Paramount Pictures owned a ranch in the area used for filming Westerns. To obtain a post office of its own the residents were required to choose a one word name, and in 1927 chose a misspelling of the last name of Pierre Agoure, a local Basque man and French immigrant who had settled in the area in 1871 to live the lifestyle of the Mexican rancher and styled himself Don Pierre Agoure, accordingly. Agoure was a successful sheep herder and had a reputation as a swashbuckler. His name was chosen for the post office as it was the shortest name proposed.

Agoura Hills is known regionally for its live music scene and artistic originality in the alt/rap-metal scene, a fame that has given rise to such top acts as Underwood, Delve, Hoobastank, Fort Minor, and Linkin Park. This music scene was born amid the coming of age of the children of the first wave of migration into Agoura Hills, those that settled in the 1960s. The 1980s was the first boom in the music scene, but by the late 80s, as many of these original rockers moved off to college or aged, the scene quietly began to slip away. However, in the mid-1990s the music scene took off again, energized by the coming of age of the children of those who had settled in the early 1980s. But by the 2000s, much of this wave of teenagers had aged or gone to college, leaving the scene with only a shell of the energy it once had. Although the scene lives on, pushed forward by various Battle of the Bands competitions and garage concerts, the lack of a third major wave of migration to Agoura Hills. Agoura Hills is home to The Canyon Club, a highly regarded concert venue that hosts national and regional touring acts such as Peter Frampton, REO Speedwagon, X, Steel Pulse, The New Cars, Asia, Boys II Men, Which One's Pink?, Alan Parsons, and The Smithereens.