It was first created in 2001, replacing the abolished seat of Jingili, and is named after Commodore Eric Johnston, a former Administrator of the Northern Territory.

Johnston is an urban electorate, covering only 5 km2 and taking in the Darwin suburbs of Jingili, Moil, Wagaman and part of Alawa.

At the 2001 election, however, the CLP member for Jingili, Steve Balch, was defeated by Labor Party challenger Dr Chris Burns.

As it turned out, Burns was re-elected easily amid that year's Labor landslide with a substantially increased majority, though the margin didn't blow out as much as in nearby seats.

In 2018, Vowles was expelled from the Labor cabinet, and resigned on 31 January 2020, with the resulting vacancy filled at a by-election on 29 February 2020.