Miller’s resignation was announced this morning after controversy over her use of parliamentary expenses and her apology to the Commons last week, and came despite receiving the full support of the Prime Minister.
Miller was cleared of funding a home for her parents at taxpayers’ expense but told to pay back £5,800 amid accusations she had obstructed the investigation.
Pointing to Cameron claiming Miller that had "done the right thing" in apologising despite criticism that her 32-second speech to MPs was inadequate, Lewington said:
"This is an unseemly mess for Cameron. He appears to have been easier on Maria Miller than he was with some of his colleagues in the run-up to the 2010 election. Downing Street failed to recognise that her perfunctory apology to the House of Commons would not be enough."
Lewington, who was press secretary to John Major in the 1990s and is now the owner of corporate and public affairs consultancy Hanover, said: "Cameron’s script for PMQs is written already. Miller was absolved of breaking the old expenses rules which have been shown to be unfit for purpose; she was entitled to defend her reputation robustly during the inquiry; she apologised as required and the whole House recognises – including Ed Miliband - that the revised model of self-regulation does not have public confidence. It was her decision to resign but he understands it."
However, claiming the Tories’ communications effort needed to "improve dramatically", he added: "Once it decided to defend her, the party machine showed itself to be uncoordinated and chairman Grant Shapps, insufficiently heavy-weight to take on the media in full flight."
The original recommendation, made by the independent parliamentary commissioner for standards, was that Miller repay £45,000.
Lowering the amount to £5,800, the Standards and Privileges Committee nonetheless said she had breached the MPs' code of conduct by submitting "incomplete" evidence.
The findings of the investigation, prompted by a story in The Telegraph, also revealed that Miller told the commissioner investigating her that she might go over the commissioner's head to ask MPs to intervene.
But despite mounting media pressure, and criticism from within the Tories, Cameron continued to back Miller, stating on Monday "We ought to remember she was found innocent of the claim that was levelled at her at the start of this process."