Inyokern began as a community in 1908, when the Southern Pacific Railroad built the Jawbone branch to support construction of the Los Angeles aqueduct. The Jawbone branch connected Mojave to Lone Pine, California. Inyokern was originally known as "Siding 16".

In 1910, Siding 16 became "Magnolia". The community was called Magnolia until 1913, when the state notified the township that a Magnolia, Calif., already existed. The name "Inyokern" was adopted because of the town's proximity to both Inyo and Kern counties.

Highway 178, the main street of Inyokern, boasts a bicycle shop, a barbershop, a food market, and a gift shop/leather shop with goods ranging from handmade wallets to ready made saddles. There are several pistachio farms in the area that produce and distribute the nuts. The local ostrich farm sells ostrich eggs; at one time, ostrich burgers were offered on the menu of a local cafe.

Several excellent restaurants are located on Highway 178 in Inyokern.

Inyokern Airport has daily flights to Los Angeles.

Inyokern also is the portal to Ridgecrest, Death Valley, and Mount Whitney.