Former Welsh Secretary and ex-Monmouth MP David TC Davies will be Millar’s chief of staff.

Conservatives in the Senedd had just over 48 hours to nominate candidates for the contest to find the new leader, after Davies quit at lunchtime on Tuesday.

By Thursday morning, all of Millar’s 15 colleagues had endorsed him, with Sam Rowlands – who had been thought of as a potential candidate – announcing his backing early on Thursday.

Unlike in Scotland, Millar only leads the party’s MSs and is not leader of all Welsh Conservatives, despite longstanding calls for that to change.

He will be leader of the opposition, and will face Eluned Morgan weekly in first minister’s question time in the Senedd.

Millar told BBC Wales he is aiming to be the first Tory first minister.

“Wales is broken, and we’ll develop a plan to fix it and present that to the public in advance of those elections in 2026,” he said.

“I believe in freedom of choice, personal responsibility, and these are the things which I will campaign with a platform on.”

Asked if he was a sticking plaster candidate, he said: “Absolutely not.

“I’ve been involved in politics for many years,” he said. “I’ve always ploughed my own furrow, and that is what I intend to do going forward”.

The former Westminster candidate for this year’s general election said he was “absolutely committed” to the Senedd.

It would be a decision for the UK party to change it, but Millar said he had always been of the view that the Senedd group leader should be the “de facto Conservative leader in Wales”.

Millar, 48, was chief whip under Davies, in charge of Tory discipline in the Senedd.

Brought up in Towyn, Conwy, he is married with two grown-up children and now lives in Kinmel Bay.

He is arguably the most senior Welsh Conservative still in office who is not the outgoing leader and is known for making robust contributions in the Senedd, particularly on the Welsh NHS when he was the party’s health spokesman.

His website says Millar worked as a manager for an international charity supporting persecuted Christians before he joined Cardiff Bay politics.

The MS suffered a setback in late 2020, when he temporarily quit his front-bench after he and three other Senedd members were seen drinking on Welsh Parliament premises during a pandemic pub alcohol ban.

Millar returned as chief whip after the May 2021 Senedd election and the four politicians were cleared of breaking the Senedd’s code of conduct.

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Millar will face questions about where to take the party next as the Welsh Conservatives prepare for the 2026 Senedd election, and after a disastrous general election where they lost all their MPs.

A recent opinion poll put the Tories in fourth, behind Plaid Cymru, Labour and Reform.

Davies’ downfall was prompted by concerns in the Senedd and elsewhere in the Tories about the party’s direction.

Supporters of Davies believed he should head into more of a Reform-style direction. His detractors wanted to see him offer a broader alternative.

Stories about disputed claims Davies had made about halal meat in a school, and a social media message where he asked if people thought the Senedd should be abolished – the party has officially supported devolution for many years.

Some of the Tory’s MSs allegedly told Davies to quit last week. In response he called a vote of confidence, which he won only narrowly.

Former Downing Street communications director to Boris Johnson, Guto Harri, said the challenge for the Conservatives was “not to swap one leader for another”, but “to position the party to offer itself as an alternative government in Cardiff to Labour”.

“Let’s get back to what it is to be a Conservative. It’s not to be an eccentric crowd pleaser, or a lobbyist for farmers, though they’re part of the mix.

“It’s to go back to advocating a small state that takes less of your money.”

He said Millar needed to bring forward “a lot of talent”, including former Tory MPs. “I wouldn’t waste Stephen Crabb, I wouldn’t waste David TC Davies,” he said.

In response to the election, a Conservative source said they thought it showed “lack of ambition that the Senedd group has for Wales”.

“If Darren Millar is the answer, what was the question?”

A Welsh Labour spokesperson said: “Voters have already rejected Darren Millar and his colleagues at the general election. Instead of trying to understand why, they are papering over the cracks.”

Reform UK Wales spokesman, Oliver Lewis, said: “The simple fact is, Darren Millar has been an MS since 2007 and has been nothing but ineffective in opposition, just like every other Welsh Tory.”

Plaid Cymru leader Rhun ap Iorwerth congratulated Millar but said he takes the job “at a time of chaos and infighting in his party, and with the Tories having failed to offer any credible solutions to the challenges facing Wales”.

A Welsh Liberal Democrat spokesperson added: “In July Welsh voters delivered their devastating verdict on the Conservatives, booting out every single Tory MP in Wales. Re-arranging the deckchairs in their Senedd group isn’t going to make anyone forget their record of incompetence, sleaze, and failure.”