The civil service is at a low ebb. Morale is at rock bottom and ministers are moaning, but the worst thing is the realisation in Whitehall that prime minister David Cameron’s criticisms contain a grain of truth. And it’s all the fault of local government!

The problem has been building for some time, and amounts to a veritable crisis in the way we are governed in England. The complacency of the political and administrative class at the impending break-up of the UK is both amazing and entirely consistent with the defeatist mood.

During the Blair-Brown years, ministers’ enthusiasm for targets and – often naïve and uninformed – passion for ‘delivery’ kept the show on the road.

An adept Cabinet secretary – Gus O’Donnell – maintained that the machine still worked as, of course, it does in such traditional arenas as defence and the organisation of royal ceremonials.

But now the wheels have visibly come off the cart. The capacity of officials has been tested well past its limits, in complex legislation and administrative reorganisation.

The shambles around plans to abolish the Audit Commission is highly illustrative – it is not just an issue of communities secretary Eric Pickles’ petulance, but civil servants’ lack of core understanding on how things fit together.

As, in recent years, political attention as shifted to public services, the civil service has failed to come to terms with the changes. Successive reports have shown their departments’ unwillingness to rework their relationship with the arm’s-length bodies which carry vital services – think of the Environment Agency.

But the dog that keeps barking, without anyone wanting to let him off the chain, is elected councils. Is significant autonomy for local authorities really compatible with the Whitehall that we have known since 1945?

The answer is clearly, no. And that is one of the reasons why, in private and often without the thought being fully formed, the civil service is in an existential spin.

Curiously, the importation into Whitehall of many senior former council executives may even have made things worse.

This ought, therefore, to be a moment of opportunity for local public managers to be in the ascendancy, assertive and confident. It’s a time when they ought to be asking fundamental questions about the future of the civil service, perhaps even the very existence of a separate cadre of public managers ‘at the centre’, itself a highly-ambiguous and misleading idea.

But there is, I fear, not much sign of that. Local authority chief executives are running scared after Mr Pickles’ populist attacks.

Health management is in uproar, as executives focus on getting by. Attention is being diverted – deliberately? – by gimmicks such as the Big Society.

Most managers concentrate on keeping the show on the road, which is admirable. But by not looking up at what is happening at the centre, are we in danger of missing what ought to be a chance to break open the myths and assumptions that have surrounded Whitehall for so long?

Now ought to be the time for some big thinking. Political focus on services is not going to fade, even if Mr Cameron’s plans to shrink government are realised.

Emerging agendas, in social care and education, demand renewed attention to central-local links, however provision may be spread among public, private and third sector organisations.

Do we need a separate ‘civil service’; any longer? Why not a more unified public service? Or is the logic of the Cameron plans the break-up of the entire pattern of recruitment?

At the very least, the shape and staffing of the domestic departments of government, communities, education, and health need thorough reshaping, with ‘delivery’ as the unifying theme.

What surely can’t survive this crisis is the idea of ‘mandarins’, and the myths of civil service excellence, intelligence and reliability. It’s up to local public servants, amid the chaos and financial stringency, to seize their chance to effect permanent revisions in the way we think about central government.

David Walker is former director of communications at the Audit Commission