Boris Johnson has accused Britain's ally, Saudi Arabia, of engaging in "proxy wars" in the Middle East.
The Guardian newspaper has published footage in which the foreign secretary talks of politicians "twisting and abusing religion" for political gain.
He said Saudi Arabia and Iran were "puppeteering" because of a lack of strong leadership in the region.
PM Theresa May's spokeswoman said his comments about "proxy wars" were not the position of the government.
The spokeswoman said that Mrs May wanted to strengthen the relationship with Saudi Arabia, saying, "we are supporting the Saudi-led coalition in support of the legitimate government in Yemen against houthi rebels".
She said: "Those are the prime minister's views - the foreign secretary's views are not the government's position on, for example, Saudi Arabia and its role in the region."
She said Mr Johnson would be in the region this weekend and it would be an opportunity for him to set out the government's position on relations with Saudi Arabia and others in the region.
Asked whether the prime minister had full confidence in Mr Johnson as foreign secretary, the spokeswoman said "yes".
In the footage from last week, Mr Johnson said: "There are politicians who are twisting and abusing religion and different strains of the same religion in order to further their own political objectives.
"That's one of the biggest political problems in the whole region. And the tragedy for me - and that's why you have these proxy wars being fought the whole time in that area - is that there is not strong enough leadership in the countries themselves."
The foreign secretary told the Med 2 conference in Rome: "There are not enough big characters, big people, men or women, who are willing to reach out beyond their Sunni or Shia or whatever group to the other side and bring people together and to develop a national story again.
"That is what's lacking. And that's the tragedy," he said, adding that "visionary leadership" was needed in the region.
He went on: "That's why you've got the Saudis, Iran, everybody, moving in and puppeteering and playing proxy wars."
The BBC's diplomatic correspondent James Landale said the emergence of the comments would be "awkward if not embarrassing for the foreign secretary".
"Once again Mr Johnson's use of language is causing headlines that his diplomats will need to explain," our correspondent said.
The video has emerged as Prime Minister Theresa May returns from a visit to the Gulf where she had dinner with the leaders of Saudi Arabia, Kuwait, the United Arab Emirates, Qatar, Bahrain and Oman.
The Guardian said the remarks flouted a long-standing Foreign Office convention of not criticising their allies in public.
Robert Lacey, a historian and author of the Kingdom and the House of Saud, said that while he agreed with Mr Johnson's comments, he questioned whether he should be saying them about an ally.
He told BBC Radio 4's Today programme that he believed it was a gaffe and that Mr Johnson was acting more like a journalist.
It was quite clear Mr Johnson had departed from the Foreign Office brief, he added.