The veteran europhile cabinet minister told a meeting of Tory MPs on Monday afternoon that most Conservative ministers were in favour of Britain staying in the EU.
The gathering in parliament also heard from Tory police minister Damian Green, who warned his colleagues that the British public would vote to leave the union if pro-EU Conservatives decided to "keep quiet".
Clarke reassured the MPs: "It's certainly the case that in the ministerial ranks of the Conservative Party, the pro-EU sentiment is in the majority, Damian and I may be outliers, but we are not by far the only ones inside and outside the cabinet."
He said the suggestion that the Conservative Party was now dominated by eurosceptics who wanted to quit the EU was false and that the orthodoxy among Tory MPs was to stay in.
"The price of orthodoxy is being less newsworthy than some of my more strident, and dare I say, more occasionally eccentric colleagues, who I've seen become household names for a year or two."
He added: "It distorts the impression that you get. It's just that they are more newsworthy."
The meeting, hosted by the Conservative European Mainstream group, was attended by pro-EU MPs including former environment secretary Caroline Spelman and prominent backbenchers Margot James, Laura Sandys, Nicolas Soames and the chair of the foreign affairs committee Richard Ottaway.
The group has decided to relaunch in response to the perceived dominance of eurosceptic Conservative voices ahead of the European elections in May and the proposed 2017 in/out referendum.
Over the weekend David Cameron set out seven "specific changes" he wanted to make to Britain's relationship with the EU - before campaigning for Britain to stay in the union.
Spelman, who was sacked as a cabinet minister by Cameron in September 2012, also defended the group from suggestions that it did not in fact represent the mainstream Conservative opinion on Europe.
"We chose to use the word 'mainstream' because we take the position of the prime minister. If that isn't the mainstream position I don't know what is," she said.
Green, who opened the meeting, said pro-EU Tories needed to start making more noise. "I don't want to hand democracy over to those who want us to pull out of Europe. I am a democrat. I believe in arguing my case in front of the public," he said.
"If we are to get a 'Yes' vote in the referendum to come in the next parliament, we need to start making the arguments now. We mustn't wait until the campaign itself.
"It is easy for those of us who are broadly speaking pro-European inside the Conservative Party to decide it's always easy to keep our head down and keep quiet, this is exactly not the time to do that."
Green added: "You simply have to as yourself at this delicate, fragile, time in the world, whether you think we would have more or less influence in America, in China, in Germany, if we had pulled out of the EU. It is palpably obvious we would have less influence in the world."