Johnston was essentially a reconfigured version of one of the original electorates in the Northern Territory, Jingili, which had been held by the Country Liberal Party for its entire existence and was the seat of the Territory's second head of government, Paul Everingham. At the 2001 election, however, the CLP member for Jingili, Steve Balch, was defeated by Labor Party challenger Dr Chris Burns. Burns' victory was part of an unexpected Labor wave that swept through northern Darwin, allowing Labor to win government in the Territory for the first time. The area's CLP voting history led many commentators to suggest that it was likely to revert to the CLP at the 2005 election. 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. Burns retired at the 2012 election, and the seat was retained for Labor by former cricketer Ken Vowles with only a small swing against Labor. Vowles consolidated his hold on the seat amid Labor's massive landslide in 2016. 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.