WASHINGTON — The racial strife roiling the country and its politics has reached an unlikely redoubt of social conservatism, Jerry Falwell Jr.’s Liberty University.

Blackface and Ku Klux Klan imagery tweeted by Mr. Falwell, who tolerates little dissent at the evangelical university he leads, has spurred staff resignations, demands for his firing by influential alumni, an incipient boycott and a raucous protest in the university’s home of Lynchburg, Va., over the past week.

So heated was the response that on Monday, Mr. Falwell, the university’s president and a vocal ally of President Trump, did something rare for him in the heat of a controversy: He apologized for a May 27 tweet in which he mocked the social-distancing orders of Virginia’s Democratic governor, Ralph Northam. In that tweet was the image of a mask on which was emblazoned the photo from Mr. Northam’s medical school yearbook of a man in black face and another in Ku Klux Klan robes, one of whom might be Mr. Northam.

“After listening to African-American L.U. leaders and alumni over the past week and hearing their concerns, I understand that by tweeting an image to remind all of the governor’s racist past, I actually refreshed the trauma that image had caused and offended some by using the image to make a political point,” Mr. Falwell said in a statement and on Twitter. “Based on our long relationships, they uniformly understood this was not my intent, but because it was the result, I have deleted the tweet and apologize for any hurt my effort caused, especially within the African-American community.”

It is not clear whether the overture — as much another jab at Mr. Northam as an olive branch to Mr. Falwell’s critics — will defuse the controversy.

“Your actions have shown you really don’t care about the black community, and that’s sad,” Keyvon Scott, an online admissions counselor who had resigned in protest, said upon learning of Mr. Falwell’s apology. “You can’t say this is a Christian university, but then everything that comes out your mouth is about Trump.”

The tweet in question came after months of criticism over Mr. Falwell’s decision to reopen Liberty University after spring break, despite the coronavirus pandemic, and of his mockery of social distancing orders.

“I was adamantly opposed to the mandate from @GovernorVA requiring citizens to wear face masks until I decided to design my own,” Mr. Falwell wrote above the blackface and Klan image. “If I am ordered to wear a mask, I will reluctantly comply, but only if this picture of Governor Blackface himself is on it!”

At least four black faculty and staff members resigned in protest, including Mr. Scott and Quan McLaurin, who was Liberty’s director of diversity retention. Players on Liberty’s popular football and basketball teams have had fraught meetings with coaches and staff to discuss George Floyd, a black man whose death in police custody has roiled the nation, and the Falwell controversy.

Mr. Scott, who graduated from Liberty, said he now faces financial uncertainty because “people take one look at Liberty University on my résumé, and I always get asked the same question: Why would you go there?”

A regional broadcaster owned by an African-American businessman and Liberty alumnus threatened to no longer run Liberty advertising or content. And the larger Liberty alumni world showed a dissident streak unheard-of in the school’s nearly 50-year history.

“It has become obvious to many that your heart is in politics more than Christian academia or ministry, so we would encourage you to leave the position of school president and pursue politics full time,” said an open letter signed by 36 prominent African-American alumni, including several National Football League players. “Your statements hurt the ability of Liberty alumni to obtain jobs and have a voice in the culture. Having the school’s name on a résumé can be a liability to many of our graduates.”

The letter was turned into a petition on change.org, signed by nearly 37,000 people as of Monday.

The tumult has spread into town. Josh Read, owner of Lynchburg restaurant Fifth and Federal, tweeted his appreciation of Mr. Falwell’s face mask idea, saying, “We would offer them to our staff as a mask option!” An ensuing protest May 31 turned violent, when demonstrators threw rocks and debris at the restaurant and neighboring businesses, injuring police officers.

Mr. Read later apologized, saying: “We love all of our neighbors and people in this community. We’re just really saddened to see how badly they were hurt.”

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Credit…Amanda Andrade-Rhoades/Agence France-Presse — Getty Images

Before Monday, Mr. Falwell had shown no remorse. He promoted the mock face mask again in an interview with the conservative television host Eric Bolling on May 27: “I hope everybody buys one.”

The uproar is more remarkable in light of Mr. Falwell’s tight control over Liberty and his intolerance for dissent. Liberty’s administration controls the content of the school newspaper. Faculty do not have tenure, and renew their contracts from year to year. And Liberty without a Falwell in charge would be a sea change for a school almost synonymous with the name.

The university was founded by Mr. Falwell’s famous father as a bastion of social conservatism, one that was unabashedly combative as it trained what it called “Champions for Christ.” Under the family, the university has grown from a modest Baptist college to a giant with cash investments and endowments of nearly $2 billion, nearly 46,000 undergraduates and a campus that sprawls across Lynchburg and neighboring communities in Virginia. Total enrollment, including online students, exceeds 100,000.

But this time, dissent ran deep. Even Mr. Falwell’s wife, Becki, chastised him. “I’m not wearing that mask, and I don’t approve of Jerry’s tweet,” she said on the Eric Bolling broadcast as Mr. Falwell laughed.

“We’ve extended a lot of grace and looked past a lot of things, but when we saw that tweet with the blackface and the KKK on it, we said enough is enough,” said Eric Carroll, pastor of the Ascension Church RVA in Richmond and a 1991 Liberty graduate.

After Mr. Falwell’s apology, Mr. Carroll said: “You can look at this one of a couple of ways. You can say, ‘Wow, he succumbed to the pressure, blah blah.’ I choose to believe he recognized the fact that he hurt some people. It took some time and some nudging, but his heart got right.”

He said there was no word on whether Mr. Falwell would meet with the organizers of the open letter. They reiterated that request by letter late Monday, adding that they would like to see Liberty’s administration “surround yourselves more with ethnically diverse pastors and advisers.”

The anger over the blackface tweet cannot be unraveled from Mr. Falwell’s contentious decision to reopen the campus after spring break, which Mr. Northam responded to by placing further restrictions on in-person instruction. Mr. Falwell reacted to coverage of his decision by lodging trespassing charges against journalists who visited the campus and threatening news media outlets, including The New York Times, with lawsuits.

Liberty students, parents and alumni have posted hundreds of messages on Facebook and Twitter objecting to Mr. Falwell’s recent behavior, some under the hashtag #LUDeservesBetter. Calum Best, a recent Liberty graduate, posted a manifesto on Facebook encouraging the Liberty community to lobby its board of trustees to censure him, and it was shared more than 700 times. Past controversies involving Mr. Falwell have not moved the board, which is composed of Falwell supporters and Mr. Falwell himself.

After talking with players and staff, Hugh Freeze, Liberty’s football coach, issued a statement on Twitter calling for unity. Ritchie McKay, Liberty’s men’s basketball coach, tweeted a statement that said in part: “The Liberty Flames men’s basketball players and staff are united in opposing PREJUDICE, BIGOTRY and RACISM. We’re against all intents associated with those three affronts to human dignity.” Mr. Falwell retweeted the statement.

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Mr. McKay, who is black, said in an interview: “I wanted to talk to our guys, the people in our family and our staff, and I wanted to pray as I usually do. I felt like people would hopefully unite in a season like we’re in with Covid, the effect of it on our economy and what happened to George Floyd.”

Of Mr. Falwell, he said: “I feel really good about what he’s done on our campus. Leadership styles are different. This is a great place to work, and our guys are having I think a life-shaping experience.”

Black alumni who signed the open letter were less sanguine.

After the apology, Andre Whitehead, the chief executive of Whitehead Media Ventures, which runs a network of Virginia regional broadcasters, canceled a news conference in Lynchburg on Monday to announce that his company would no longer air Liberty advertisements and content.

In an interview before the apology, Mr. Whitehead, a 1988 Liberty graduate, said he had called Mr. Falwell personally last week asking him to apologize, delete the tweet and meet with the four organizers of the open letter.

“Just because you may have the right to say something does not mean that it’s the right thing to say,” Mr. Whitehead said he told Mr. Falwell. “Any references to a Klan outfit or blackface is offensive to people of color, no matter how you couch the reasons for saying these things.”

What did Mr. Falwell say?

“I’ll just say that he didn’t agree with my view,” Mr. Whitehead said. “I hope he changes his mind, and reconsiders.”

Kitty Bennett contributed research.