But it was the divide in U.S. foreign policy between President Trump's comments and his administration's actions that underlaid the contentious hearing, with Pompeo at one time seeming to suggest that the administration's actions mattered more than Trump's words. He was quick to correct himself later, saying that he misspoke, but blasting what he called Democrats' "glee" at his mistake and their efforts "to make a political point from that."
"That's silliness. This president runs this government. His statements are in fact U.S. policy," Pompeo declared in a particularly heated exchange with the top Democrat on the Senate Foreign Relations Committee, Sen. Bob Menendez, D-New Jersey.
While Pompeo dismissed Menendez's concerns as a "political soliloquy," they were shared by the committee's Republican chair, Sen. Bob Corker, R-Tennesse.
"The policies that we're putting in place, in many cases, are stronger," Corker said. "It's the president that causes people to have concerns... It's the president's actions that create tremendous distrust in our nation, among our allies. It's palpable."
Although he is from the same party as the president and secretary, Corker has often been critical of Trump, but Wednesday's words were some of his strongest words yet -- questioning Pompeo on why the president has welcomed dangerous proposals from Putin as an "incredible offer" or sowed doubt in the U.S. public about the importance of NATO and America's commitment to it.
He said the committee was "filled with serious doubts about this White House and its conduct of American foreign policy," and added, "We really need a clear understanding as to what is going on, what our president is agreeing to, and what our strategy is on a number of issues."
Pompeo shot back with his signature loyalty to the president: "I disagree with most of what you said here. You somehow disconnect the administration's activities from the president's actions. They're the one and the same."
The verbal tussle between the Trump administration's top diplomat and the leading Republican senator on foreign policy was notable, but their disagreement was the same one that many senators had with the former Congressman and CIA Director.
Pompeo repeatedly referenced a list of Trump administration actions to counter Russian aggression, from sanctions to diplomatic expulsions to increased military spending. But senators countered with the president's own comments, praising Putin, calling into question the U.S. commitment to NATO allies, and blaming Democrats, Special Counsel Robert Mueller's investigation, or former President Obama for the low point in U.S.-Russian relations, not Russian misbehavior.
"If President Obama did what President Trump did in Helsinki, I'd be peeling you off the Capitol ceiling. Please," Menendez said angrily at the hearing's close.
When Corker offered Pompeo the chance to respond, he said grimly, "Not a word."
Senators probed for answers on what Trump and Putin discussed, but Pompeo wouldn't answer many questions, including about whether Trump and Putin discussed easing sanctions or whether Trump asked Putin to withdraw from Crimea or eastern Ukraine. While he said he was fully debriefed by the president, he repeatedly dismissed questions, telling senators that "presidents are permitted to have conversations with their cabinet members that aren't repeated in public."
But he did point to some specific outcomes, including coordination on counterterrorism, a possible deal to help Syrian refugees return, and restoring a Russian-American business council.
While senators from both parties criticized the administration for engaging with Putin despite his aggression in Europe and in cyberspace, Pompeo told the committee it was important to continue to keep channels open: "Now is the time for direct communication in our relationship in order to make clear to President Putin that there is the possibility, however remote it might be, to reverse the negative course of our relationship."
Even as Trump has cast doubt on whether Russia interfered in the 2016 presidential election, Pompeo said he made clear to Russian officials in Helsinki that there will be "severe consequences for interference in our democratic processes."
"President Trump is well-aware of the challenges that Russia poses to the United States and our partners and allies. He has taken a staggering number of actions to protect our interests," Pompeo added, although several senators pressed him on Trump's own comments that cast doubt on that -- including a tweet over the weekend that called Russian interference "a hoax."
There were some moments of agreement though.
Pompeo agreed that new sanctions on Russia would be appropriate "if we can find the right places, the right leverage points that will actually make a difference to Russia." And shortly before the hearing started, Pompeo issued a statement to say the U.S. still opposes Russia's "attempted annexation" of Crimea, which violates "a bedrock international principle shared by democratic states – that no country can change the borders of another by force." Trump had previously left the door open to the U.S. recognizing Crimea as part of Russia, telling reporters, "We're going to have to see."
Over six weeks since the Singapore summit, with few demonstrable signs of progress on North Korea's denuclearization, Pompeo also faced questions about the administration's diplomatic push with North Korea. Even though he confirmed that North Korea continues to produce fissile material that can create nuclear bombs, he said there had been progress towards denuclearization.
In particular, Pompeo welcomed new satellite images released Monday that showed North Korea taking steps to dismantle key facilities at a missile testing site, saying the U.S. was tracking the "disassembly" of the site and calling it "a good thing" and "steps forward."
But he conceded, "There's an awful long way to go... There remains a great deal of work to do. It will be highly contested – that is, the modalities, the means, the timing of this will be things that I'm confident we'll be discussing for a period of time."
Among those potential challenges, he refused to say whether the North Koreans are working on submarine-launched missiles or any other nuclear technology while in an open setting.
While the Trump administration tore up the "strategic patience" that was the Obama administration's policy, Pompeo added that because of those timelines they "are engaged in patient diplomacy, but we will not let this drag out to no end."
It's unclear how long they are willing to give talks, but Pompeo said they are still aiming to achieve "complete denuclearization" before the end of Trump's first term, if not sooner.
Pompeo visited Pyongyang less than a month after the summit, but he was denied the meeting with Kim that the White House said he would have, and the North Koreans bashed the U.S. for making "gangster-like" and "cancerous" demands in their two days of meetings.
Downplaying those tensions, Pompeo told senators the U.S. knows the "truth" of those meetings and talks continue.
ABC News's Sarah Kolinovsky contributed to this report.