Trevor Phillips clashed with Oliver Dowden after telling him voters no longer know what the Tory Party stands for.
The Sky News presenter asked the deputy prime minister “who are you” following fresh controversy over comments by high-profile Conservatives.
Former prime minister Liz Truss was criticised for appearing alongside Steve Bannon at a right-wing conference in America, while Suella Braverman was condemned for claiming that “Islamists” now run the country.
And Lee Anderson, the former Tory deputy chairman, was stripped of the Tory whip after he refused to apologise for comments about Sadiq Khan.
The controversies come against a backdrop of last Wednesday night’s chaotic vote on Gaza in the Commons, when Speaker Lindsay Hoyle controversially allowed a Labour amendment amid fears of a backlash against MPs by pro-Palestine campaigners.
On Sky News this morning, Phillips told Dowden: “Right now we don’t quite know what Tory Party we’re being asked to vote for.
“Is it the old school, genteel ‘one nation’ Conservative Party that I think most people associate with Oliver Dowden?
“Or is it this modern, brash take no prisoners Conservatism of Lee Anderson, Liz Truss and Suella Braverman? Who are you?”
But Dowden said there was no contradiction between the two positions.
He said: “What I’ve been trying to get across to you in my answers, and maybe I’ve not been doing it very well, is to say that I don’t think it’s incompatible being a one nation Conservative as I am and many others have been.
“But calling out these threats and intimidation actually, as a one nation Conservative who believes in our nation and defending the values of this nation, one of the most precious values in free speech, free expression and our parliamentary democracy.
“And we have seen in the past week threats to that parliamentary democracy.”