For many years, historical accounts of Australian Federation ignored the distinctive ideological origins of the Australian Constitution. From the mid 1980s until the 2000s, however, a generation of historians remembered how the Australian drafters built a distinctive constitutional democracy that combined trust in parliament with a direct constitutional role for a plural ‘people’: the people of Australia and the people of the states. Drawing on Chartist and American ideas of popular sovereignty, this system of popular political constitutionalism textually guarantees that ‘the people’ can ‘directly’ choose both houses of parliament, break deadlocks between these houses and make constitutional law. The definition of ‘the people’ in this distinctive form of constitutional democracy was, however, racially exclusive. In particular, First Australians were excluded from the plural people of Australia. This intellectual history of the Australian Constitution, however, has had remarkably little impact on constitutional interpretation and discourse. This paper will begin the process of examining those implications. First, it will show how this history provides important contextual support and direction to the implied limitations on parliamentary power that stem from the constitution’s guarantee of representative democracy in sections 7 and 24 of the Constitution. Second, it will demonstrate how it aids in better understanding Australia’s unique constitutional system. To date, this system has remedied the racist roots of the original constitutional definition of the people largely through legislative reform. The constitutional recognition of First Australians is a critical step in acknowledging that First Australians are a distinct part of the plural Australian people. In the aftermath of the failure of the First Nations Voice to Parliament proposal, meaningful constitutional recognition for First Australians must address their structural exclusion from the plural Australian people.