He led this from the front thinking UKIP could be defeated – a Tory win these days – but is now reeling from a backfire that will resonate throughout his Cabinet, panicked backbenchers and soul-destroyed party activists.
Ed Miliband has fared little better, as this seat should be Labour territory.
They have emerged with bloody noses from a double knock-out courtesy of Nigel Farage and Britain’s disaffected voters.
What is clear is that neither of the main political parties has a strategy for dealing with UKIP or a clear political message to give to the electorate on how they would reform Europe – and by that, I mean immigration.
For Cameron, today’s result is a huge personal blow and will only encourage those in his parliamentary party to jump ship to UKIP.
He chose this to be a high profile campaign led from the front, and raised the stakes by saying the Conservative machine would throw everything at it.
The political judgement that will come to haunt him is that he felt this was recoverable – a line in the sand after the disaster of Clacton. But instead, he threw it all away.
There will be talk of Cameron reading the riot act to his pollsters and strategists who followed him into the lions' den five times over recent weeks.
But the PM’s self-confidence was not based on polling or focus groups.
It was based on political survival at a time when Conservative HQ was in blind panic among rumours of more high profile defections and resistance from many of his own backbenchers to campaign in a seat that they felt was lost.
Miliband knows that his parliamentary party cannot pander to the right on this issue, but whether he likes it or not, that is where Middle England is.
His formerly high-profile American political strategists don’t seem to be aiding him effectively, either.
These are people who have gone from giving key messaging to Obama on global matters in Washington DC to trying to figure out Farage for Miliband in Rochester.
That they are still in post of their own volition is a miracle.
The lack of confidence within Labour was shown in stark relief by the debacle of Emily Thornberry’s tweet, the mishandled comms response, and finally her resignation from the shadow cabinet.
Both Cameron and Miliband look and act like leaders who have stopped listening to their voters. There is panic in both camps.
But if they adopt short-sighted political posturing on the scale of Cameron's Rochester misjudgement, they will reap the headlines and voter response that they deserve.
They need a compelling and positive story about the benefits of the EU and the dangers that our public services might face if the hard-right extend their influence further.
Middle England might listen to them – but the final problem the main parties have is that right now, Middle England doesn’t really want to.
Nick Williams is head of public affairs for FleishmanHillard London