In the early 20th century, stock routes were prevalent throughout Central Australia. In 1976, the Aboriginal Land Rights (Northern Territory) Act was passed, which became the mechanism allowing Aboriginal people in the Northern Territory to claim rights to unalienated Crown land based on traditional occupation and cultural connection.

On pastoral leases north of Alice Springs, the only Crown lands were the stock routes, so Aboriginal people with traditional connections to these lands placed land claims on the stock routes. From these land claims sprang outstations. Also known as homelands, outstations were set up to provide residential accommodation and essential services for the Traditional Owners to live on their country.

Ingkerreke Outstations Resource Services Aboriginal Corporation was developed and incorporated in 1985 by the Traditional Owners of the land to the north of Alice Springs to provide services to the new outstations in this area. For the first 20 years of its operations, Ingkerreke delivered fundamental support services to outstations. During this time, it also developed an excellent capacity for delivering quality building services, particularly in remote locations. As a result, in financial year 2004/5, the Directors of Ingkerreke Outstations Resource Services established a separate commercial operation, Ingkerreke Commercial, to capitalise on these skills and experience. Over time, Ingkerreke Commercial became a leading wholly-commercial Aboriginal Construction and Metal Fabrication supplier in Central Australia. In 2015, Ingkerreke Commercial Pty Ltd began trading as a stand-alone, aboriginal-owned commercial business.

In the past, Ingkerreke Outstations Resource Services also coordinated land management services on Aboriginal Land Trusts within a 50-100km radius of Alice Springs, mainly focusing on the Iwupataka Land Trust west of Alice Springs. This area includes Standley Chasm and other deep gorges which provide habitat for many rare plant species, as well as vulnerable or threatened animal species, such as the Black Footed Rock Wallaby. The Ingkerreke Rangers were funded through the Working on Country program from 2007-2013 and employed local Aboriginal people to collect baseline data on land, flora and fauna to be used in fire, feral animal and weed management plans. As a result of this program, five local Aboriginal men obtained positions with NT Parks and Wildlife.

In late 2020, Ingkerreke Outstations Resource Services Aboriginal Corporation Members changed the Corporation name to Ingkerreke Services Aboriginal Corporation. Ingkerreke Services continues to deliver services to 46 homelands, operating as a grant-funded Corporation and a parent organisation to Ingkerreke Commercial Pty Ltd. In addition, where possible, Ingkerreke Services supports homelands residents to develop their own enterprises, through advocacy; innovation; grant application/administration; or their own service delivery.