In a lecture on the role of the public service, Mr Pezzullo said public servants must navigate remaining apolitical in a political sphere and ensure they are always ready and willing to serve the government of the day.

While public servants must serve in the public interest, it is up to the elected government to decide what the public interest is, Mr Pezzullo said in an address to the Institute of Public Administration Australia on Tuesday.

"It would be mortally dangerous to our system of government for the public service to come to possess an aggrandised conception of its role in the proper processes of government – as the ultimate guardian of 'the public interest', located outside of the political process."

"There is no legitimate basis for contending that unelected officials have any purportedly 'supranational' responsibility as custodians of the 'public interest', somehow separately identified from the domain that is termed too often to be that of 'politics'."

Democracy means that only ministers can decide on major issues of policy, even though it is only the public service that can give the best advice to government.

"A public service which does not see itself conjoined to this endeavour has lost its way," Mr Pezzullo said.

An apolitical public service is one of the key institutions of the Westminster system of government, Mr Pezzullo said, but public servants can't avoid politics.

"There is no inconsistency in the [Australian public service] being both responsive to the government, on the one hand, and simultaneously existing as an apolitical career service to enhance the effectiveness and cohesion of Australia’s democracy."

In the lead up to the next federal election, and less than a month after his department was raided by the Australian Federal Police over possible leaks about Home Affairs Minister Peter Dutton and the au pair scandal, Mr Pezzullo said public servants must be ready to switch allegiance when governments change, but also maintain discretion.

"While the public service exists primarily to serve the government of the day, it also maintains a jealous watch on the papers and records of earlier governments, while also maintaining an underlying capability to serve future governments, including by way of an ability, and a disposition, to switch its loyalty to a newly elected government at the appropriate moment," Mr Pezzullo said.

"Elected governments are fully entitled to expect loyalty and dedicated service from its officials."

Ministers and "seasoned" staffers, the secretary emphasised, understood that career-based public servants must use discretion in respect to previous governments while only serving the government of the day.

"Our vocational calling is to assist governments to be better than they would otherwise be, but not to seek to make them different governments, which perhaps might conform to our preferences and outlooks."

"If we have a different interpretation of the 'public interest', and feel strongly enough about it, we should resign our positions as public servants and run for elected office ourselves."

The powerful secretary once dreamed of becoming a history professor before joining the public service, and said he was concerned that even senior public servants didn't pay enough attention to the structures and traditions of British constitutionalism.

"I am becoming concerned, and increasingly so, at the paucity of knowledge of these traditions and  understandings amongst public servants – even relatively senior ones. We need to do more to teach and inculcate this world view."