Larrakeyah is named after the Larrakia people, who inhabited the area for thousands of years prior to European settlement, and who are the traditional custodians of the land where the city of Darwin was built.

In 1913, the Kahlin Compound was established as a segregated camp where Aboriginal families removed from their communities were forced to live in rudimentary structures while receiving a western education, or providing cheap labour for white residents.

From 1924, children from the compound were removed from their families to the nearby Myilly Point Half-Caste Home where an inquiry on behalf of the Administrator of the Northern Territory, Frederic Urquhart suggested they could be disciplined and integrated with white society.

The rest of the suburb is predominantly residential, with some high-rise development in the Cullen Bay area, on the fringe of the Darwin CBD and overlooking The Gardens.

There are a number of serviced apartment developments and accommodation businesses in the suburb, owing to its proximity to the city and tourist attractions including Mindil Beach and the Casino, the George Brown Darwin Botanic Gardens, Doctor's Gully and bars and restaurants at Cullen Bay.

These are rare examples of tropical architecture from the period that relied on natural ventilation for cooling, surviving both the Japanese bombing raids and Cyclone Tracy that devastated many older buildings in the city.

[10] The Sealink ferry terminal is located at the end of Marina Boulevard in Cullen Bay, providing connections to Mandorah and the Tiwi Islands.