The Republican gubernatorial nominee ran on countering gang crime and illegal immigration and protecting Confederate history - cultural issues that Trump has made a touchstone of his presidency - but lost to Democrat Ralph Northam, 54 per cent to 45 per cent.
Ohio Governor John Kasich, (R), said yesterday's contests are a lesson to Republicans that catering to the party's conservative base with hard-line appeals and incendiary language turns off the moderate voters they need to win in states like his own.
He said his party must choose between a political message of "blaming and scapegoating" or a more hopeful pitch centered around everyday issues like health care and the economy.
"This is a repudiation of the politics of narrow," Kasich said. In an apparent reference to Trump's 2016 victory, the Governor added, "The politics of anger may work for a moment in time, but it does not last, thank goodness."
But other party leaders warned against drawing overly broad conclusions about Trump and his political strength from defeats in a handful of states - including two, Virginia and New Jersey, that Democrat Hillary Clinton won in the last presidential election.
"Democrats say this is a repudiation and this is an anti-Trump vote, but to me the case doesn't stick," said Robin Hayes, chairman of the North Carolina Republican Party. "Donald Trump is extremely popular in a lot of places. His promise to 'drain the swamp' resonated and still does."
Said Governor Bill Haslam of Tennessee: "When you see one night of elections, you see one night of elections. There is always natural wind at your back if you're not in the White House and wind in your face if you are."
Still, even among Trump's allies, there were complaints about the White House being disengaged and unready to deal with the party's mounting challenges.
"The White House isn't paying attention to the suburbs and there has never really been a political operation there," said Edward Rollins, the strategist for Great America Alliance super PAC, a pro-Trump group. "They have to develop a strategy where it's not just Trump alone winning, where the whole party is able to win."
Andy Surabian, an adviser to the group and an associate of former White House chief strategist Stephen Bannon, said blame cast upon Trump and Bannon for lurching the GOP to the right was misplaced.
"Establishment Republicans are blaming Trump and talking about Armageddon, but what is their alternative?" Surabian asked.
White House officials defended Trump's efforts to help fellow Republicans, noting that he has held numerous fundraisers and other events to help the party. And they argued that the best way for incumbents to navigate the political turbulence would be enacting tax cuts and other Trump policies.
"The American people expect Republican majorities to deliver on their promises of boosting our economy, cutting taxes and repealing the disastrous Obamacare law," said Raj Shah, a White House spokesman. "Nothing would help the political standing of Republicans in Congress more than delivering on the president's agenda."
Trump's friends at the Capitol said the divisions are more about style than substance. "The difficulty is, we have a president who didn't come from the Washington structure, so it's really hard for people inside the structure or outside the structure to evaluate him," Senator David Perdue, (R), said.
The fresh discord comes after weeks of escalating tensions inside the GOP. Three prominent Republican senators - John McCain and Jeff Flake of Arizona and Bob Corker of Tennessee - have publicly condemned Trump's leadership and questioned his fitness for office.
It also comes amid an exodus of House Republicans. This week alone, congressmen Frank LoBiondo, New Jersey, and Ted Poe, Texas, announced they would not seek re-election next year, joining a list of more than two dozen colleagues who are retiring or running for another office.
Democrats see many of those vacancies as ripe territory as they look to win back the House majority. Democrats will need to capture 24 additional seats next year to reach the 218-seat threshold necessary for control of the House.
Pennsylvania Congressman Ryan Costello, (R), conceded that the election results present challenges for incumbents like him. He represents a suburban Philadelphia district that Democrats are targeting aggressively in a region where Democrats won some local and county races for the first time in more than a century.
"We don't know if it'll be a wave. What we saw yesterday suggests that hypothesis has some merit, but remember, congressional districts are still one by one," Costello told reporters on Capitol Hill. "I'm very confident that I've given 110 per cent effort to this job."
Democrats are grappling with problems of their own. As celebratory and cathartic as the victories were for a party demoralised by Trump's victory, Democratic leaders know Northam's success in Virginia does not necessarily mean there will be a nationwide upswing next November.
"Virginia is a microcosm of a large portion of the nation, but it doesn't represent every community or every state," said Congressman Raul Ruiz. "We have to make sure that we are fighting for the people where they're at - in the rural and urban communities - and reflect their struggle to have better lives."
Ruiz added, "Running purely against Trump is not the full picture."
Democratic leaders have echoed that sentiment, saying the party must develop its own affirmative message and must strive to connect with voters everywhere, in particular regions where Trump remains popular.
"There remains a lot of work to do in reaching those small town or rural Democratic voters," said Senator Robert Casey of Pennsylvania. "They are the ones who need to hear from us, too. Those are the voters our party has had a problem with over the years. We need to speak to them about the lack of wage growth and the opioid crisis. We may not even win in those areas, but we could narrow the margins."
Republican strategists said the party's image has suffered from nearly a year of stalemates, fits and failures to govern, despite the party's control of both chambers of Congress as well as the White House. That is one reason the proposed tax code overhaul has taken on such urgency among GOP leaders.
Robert Dole, a former GOP Senate leader and presidential nominee, said it was premature to assess the political environment for the midterms, and that his party could improve its standing if it manages to pass major legislation.
"While I am disappointed in the overall results of yesterday's election in Virginia, I don't believe we can measure the full impact on the GOP just yet," Dole said. "If Congress passes the tax bill this year, this will help the President's popularity. As a party, we should have a better sense of where things are headed in six months or so."
Republican consultant Josh Holmes, a former chief of staff to Senate Majority Leader Mitch McConnell, said the losses should prompt the party's lawmakers to act quickly on taxes.
"It provides all the motivation they need to get something done," Holmes said. "In part, what happened is a reaction to what's not being done and a warning sign that they need to move. They don't have any choice but to do the tax plan."
But with aspects of the tax plan fluid as Republicans squabble over its details, Murphy and other Republicans said lawmakers will have to make decisions that allow them to appear independent from Trump in case the tax legislation fails to pass or the President's approval ratings decline further.
"Republican members of Congress in swing districts cannot be Trump lemmings. They have to create their own strong identities," Murphy said.
In the states, where Republicans have won control of a majority of governor offices and state legislatures over the last decade, GOP leaders said the path forward was much the same: Protect yourself.
"People get in trouble when they try to wear someone else's clothes," Haslam said. "Each candidate has to decide for himself or herself whether [Trump] is something to focus on or if they're running for governor of their state and saying, 'I'm going to run my race.' Good candidates rise or fall on their own."