It is indisputably true that the civil service exists to serve the government of the day. Constitutionally, it is an indivisible part of the executive government; it can't pick and choose which bits of policy it sees as worthy of support.
Equally, though, another core role of civil servants is to "speak truth to power," to offer unvarnished and evidence-based assessments for ministers to consider. The civil service doesn't exist simply to tell ministers what they want to hear.
Where, then, is the line between appropriately "serving" and blindly "obeying"?
To answer that question, we have to take a step back from the noise of Brexit to assess an underlying shift over the past two decades, and not just in Britain. It's a swing away from what we might call "governing in private" to "governing in public."
Where once civil servants could give their frank and fearless advice privately to ministers in the quiet rooms of Whitehall, they now find themselves drawn into a brighter light.
The anonymous mandarin of the Sir Humphrey era has given way to something more public and more confronting.
In this age of real-time leaks on social media, freedom-of-information laws, a 24/7 news cycle and select committee investigations, the room for civil servants to reflect privately has shrunk dramatically.
This does not mean that our civil servants have suddenly become Beyoncé-like bureaucrats, cultivating millions of followers on their Twitter accounts; but it does mean they face new challenges.
As they become more public, they are exposed to the perceptions of those keen to criticise what is seen as the politicisation of their position.
The late Canadian academic Peter Aucoin once highlighted a type of "promiscuous partisanship" creeping into the work of public servants in Canada under Stephen Harper's Conservative government.
Public servants were increasingly acting as agents of the government of the day, he argued, toeing the line in their dealings with citizens.
Of course, allegations of politicisation can be easier to make than they are to refute, but Aucoin's thesis reveals the degree to which the persona of administrative leaders is being tested by the new realities of modern governance.
That is not to say it's somehow novel for civil servants to be tested by politics. What is new is the extent to which that test takes place in public.
One way to draw out the contrast is to look back to the Suez Crisis of 1956.
It is now a matter of historical record that Britain and France secretly supported an Israeli invasion of Egypt in order to wrest control of the Suez Canal back from Egypt.
Having disingenuously called for an Israeli withdrawal, Britain and France followed up by sending in troops of their own on the pretext of separating the warring parties.
When asked about these events in the House of Commons, prime minister Anthony Eden insisted that there had been no foreknowledge of the Israeli invasion.
The reason this tested the civil service leadership is that the cabinet secretary, Norman Brook, knew very well that there was documentary evidence of the agreement between Britain, France and Israel. He knew this because he had been asked by the prime minister to destroy it.
"In this age of real-time leaks on social media, freedom-of-information laws, a 24/7 news cycle and select committee investigations, the room for civil servants to reflect privately has shrunk dramatically."
What is salient here is that the full extent of Brook's insight was not revealed until segments of his diary were released by the National Archives more than fifty years later. In 1956 he acted with maximum discretion in an environment of close trust with the politicians he served.
Both that level of trust and the capacity for working in secret are much diminished in the 21st century - and this is not necessarily a bad thing.
Of course, even now not all ethical challenges for civil servants are as dramatic as the one Brook faced.
Many of their forays into the public domain occur despite their best efforts, rather than from an innate desire to get involved in political battles.
Think, for example, of someone like Britain's former EU negotiator Olly Robbins, whose conversations were overheard in a Brussels bar and splashed across the newspapers the following day.
Similarly, permanent secretaries have little choice when, having been berated by select committees, they find themselves on the front pages.
But the contemporary setting also allows for more proactive interventions.
For example, former UK treasury secretary Sir Nicholas Macpherson supported the release of his advice to government during the Scottish referendum campaign on whether it would be viable to maintain a currency union with Scotland if it voted for independence. His conclusion that it would not be advisable for Scotland to be allowed to retain the pound was widely reported in the press.
This is just one episode among many that suggest the former ideal of the anonymous civil servant is no longer commensurate with the demands of modern government.
Until the 1990s, for instance, the British security services did not publicly release the names of who was leading them.
That desire for secrecy saw the British establishment go to extraordinary lengths to try to prevent a former spy, Peter Wright, from publishing his memoirs in the 1980s in the sensational Spycatcher saga - the legal battle that first brought Malcolm Turnbull's name to public notice.
Yet current director-general of MI5, Andrew Parker, freely provides media comment and travelled to Berlin in 2018 to give a speech on the current security challenges facing Europe. He is "governing in public."
Officials in charge of other arm's-length agencies have embraced an even greater licence to intervene. For instance, in 2017 the head of the UK Statistics Authority, Sir David Norgrove, publicly criticised the then foreign secretary Boris Johnson for continuing to claim that Britain would regain £350 million per week once it left the European Union. Norgrove labelled this "a clear misuse of official statistics" in a public letter of rebuke released via the authority's Twitter feed.
Is this a good thing? Is there a line between frank and fearless advice and an unwarranted attack on the government of the day? And where should civil servants draw the line in supporting their governmental masters if they are to avoid becoming "promiscuous partisans"?
Practice from other parliamentary democracies operating on some variant of the Westminster system suggests that there is room for public servants to stand their ground without bringing the institutions of government crashing down around them.
During the 2013 Australian election campaign, for example, the heads of Treasury and the Finance Department put out a media release effectively rebuking the then prime minister Kevin Rudd for suggesting their departments had provided advice on opposition financial costings.
They took care not to make an overtly political statement, simply expressing a desire to correct the public record.
Practices of public sector leadership in the United States - with its balance-of-power system of government - have long allowed for greater visibility for administrative leaders, who carry a more obvious level of public accountability for the agencies they lead.
In the age of Trump, this has dialled up to new levels of combativeness. In its most dramatic manifestations, we find confrontations like the one between the president and the former head of the FBI, James Comey.
This kind of public slugging match through the medium of congressional or Senate committees gives non-elected administrative leaders the opportunity to speak truth to power in very public ways.
Less dramatically, but just as importantly, some American leaders simply bring uncomfortable facts to public attention, knowing that in the process they will undermine the political wishes of their president.
The extraordinary story of Hurricane Dorian, with its pathway mapped out by a presidential Sharpie pen, is a case in point. President Trump had been convinced that the storm would take in Alabama - an assertion that was contradicted the same day by the National Weather Service in Alabama.
The National Oceanic and Atmospheric Administration then weighed in, saying that the National Weather Service had been wrong to assert quite so categorically that the hurricane would pass Alabama by.
Either the National Weather Service had in fact got it wrong or the National Oceanic and Atmospheric Administration took a politically expedient position. Either way, what makes it remarkable is that this three-way conversation between the president and two scientific government agencies happened in full public view.
Is something similar happening, or going to happen, in Britain? And if so, is that necessarily a bad thing? The key distinction here is between being "political" and being "partisan".
No civil servant has any business openly supporting one political party against another. But at the same time civil servants - especially at the permanent secretary level - deal with politics every single day. Policymaking always has a political element. There is no concrete divide between politics and administration.
Every comment founded in evidence-based policy is capable of being read in political ways. In the current environment, it is hard to conceive of any public statement about the potential impact of Brexit that all sides would accept as "non-political." Just as any statement about the effects of Hurricane Dorian would be read through a political lens, so any civil servant who says anything about Brexit is walking into uncharted territory.
Today's civil servants, like their ministers, operate in a noisy public square that is full of ideas, opinions and comments - wrapped in a heavy layer of antagonism and political hyper-ventilation.
But in an era of fake news, constant real-time critiques and hyper-partisan politics, having voices prepared to bring data and evidence to the table has benefits.
Civil service leaders are well placed to contribute to well-informed discussions - not in an overtly political way, but simply by providing evidence and facts about the likely impact of events on policy outcomes.
As they do so, they must also be aware that observers will seek to draw them further into partisan debates. Politicians may well take umbrage at their views and argue back - as indeed they are entitled to do. It is part of the cut-and-thrust of democratic debate. Civil servants have in fact been arguing with ministers for centuries.
That brings us back to Lord Kerslake's observation, which is not nearly as revolutionary as it at first appears. What civil servants must do is speak truth to power in frank and fearless ways. That's actually what they've always done.
In doing so they are serving the government of the day and playing a stewardship role for the country. The difference is that it now happens in more public ways and in the middle of the most turbulent period in British politics in living memory.
No one is saying it's easy.
- Dennis Grube is a lecturer in public policy at Cambridge University and an adjunct professor at the University of Tasmania and Griffith University. His latest book is Megaphone Bureaucracy: Speaking Truth to Power in the Age of the New Normal (Princeton University Press, 2019). This article first appeared in Inside Story, and subsequently appeared in the Canberra Times.