Midterm Elections Live Updates: Democrats Expand House Majority as Lead in Mississippi Senate Race Grows

That was the story of the election for Ms. Collins, the chairwoman of the Appropriations Committee and a force in the Senate for three decades.

“I was caught up in the Trump tsunami that swept away many incumbent Republican senators who have served their states well for many years and really care about our country,” she said.

The five-term Republican senator had long seemed invulnerable to the ordinary laws of politics because of her singular political brand as a New England centrist with a gift for constituent service and an ability to steer federal dollars back home. In 2008, she triumphed in Maine while Barack Obama was romping and other Republicans were falling. In 2020, it seemed like her number might be up when polls had her down against a well-funded state lawmaker, but she again won easily.

Democrats saluted ruefully in respect.

But 2026 turned out to be a different case entirely as Ms. Collins was brought down by a combination of factors, most of which were attributable to President Trump and the war with Iran. There were soaring fuel prices in a state reliant on home heating oil. The punishing tariffs the president imposed on neighboring Canada. An immigration crackdown that resulted in a fatal shooting by federal agents in one Maine community. And always the perception that she wasn’t doing enough to stand up to the president, even when she was one of the few Republicans to occasionally break with him.

“Everybody ignores the fact that I voted to convict him in the second impeachment trial,” Ms. Collins said. “What bigger break could there be? It is never enough. I want results and they want angry rhetoric.”

On top of dissatisfaction that she hadn’t distanced herself sufficiently from the president, some voters harbored resentment about her vote in 2018 to confirm Justice Brett M. Kavanaugh to the Supreme Court, given his later role in overturning Roe v. Wade.

The coming result was evident from talking to voters on Tuesday as they exited the central polling place in Bangor — home turf for Ms. Collins. Several of them said they had repeatedly marked their ballots for “our senator,” as her ubiquitous yard signs proclaimed, but they would not do so this time.

“This time,” said Deborah Hanson of Bangor, “I’ve got to try something new. Susan Collins has voted with Trump on so many things.”

“To me, it is a close thing,” said Bob Kelly, another longtime Bangor voter. “But I can’t support anybody that supports Trump.”

In rejecting Ms. Collins, Maine voters gave up a tremendous amount of influence over federal spending by turning out the woman at the helm of the influential committee that controls federal spending. It is unusual but not unheard-of for voters to reject senior leaders.

Voters in Washington State dumped Representative Tom Foley, a Democrat, when he was speaker of the House in 1994. Senator Tom Daschle, the Democratic leader, lost his re-election bid to Senator John Thune, now the majority leader, in South Dakota in 2004.

Ms. Collins leaned heavily on her role in spending as she campaigned around the state, visiting the fire stations, community projects and infrastructure improvements for which she had secured funding, noting that if she were no longer in office, that money might dry up.

“I wanted to make sure people know what their choice was,” she said.

The man who defeated her, Mr. Jackson, will be a junior member of the Senate with little ability to steer to the state anywhere near the kind of financial aid that Ms. Collins had helped win.

“What she has been able to do over the last six years is extraordinary,” said Steve Abbott, her campaign manager and longtime senior aide. “Every town you go to, you see a project that was funded and work that needed to be done. That’s an opportunity that the state has walked away from.”

Up until the end, Ms. Collins and her team had hoped they could pull out a win as they watched from a hotel suite in Bangor. They had been cheered by the “rock star” reception they received around the state, an outpouring they said was better than during some of her winning races in the past.

“We went all over the state and I’ve got to tell you, the crowds were huge, the reception was warm and the response could not have been better,” Ms. Collins said as she addressed and thanked supporters in Bangor before the results were known.

But results from the Democratic stronghold of Portland overwhelmed her.

The race was chaotic, and Ms. Collins and her advisers like to note that they basically had to run against three opponents: Gov. Janet Mills, who initially appeared to be the likely challenger before she dropped out; the oyster farmer Graham Platner, who won the Democratic primary but dropped out after sexual abuse allegations; and Mr. Jackson, who had lost the state’s Democratic primary for governor but was then selected to replace Mr. Platner on the ballot.

Democrats have been frustrated for years both by Ms. Collins herself and their inability to defeat her. They poured huge amounts of money into the campaign, trying to highlight her ties to Mr. Trump and her votes for his policies. Ms. Collins pushed back, noting her own differences with the president on the Iran war, tariffs, the immigration crackdown and safety net cuts.

Over the course of her career, Ms. Collins was at the center of many major legislative negotiations on such tough issues as gun safety, health care and, following the Jan. 6, 2021, assault at the Capitol, a bill overhauling how electoral votes were counted. Her absence in the Senate will be felt on big legislative fights. She has not missed a vote in her Senate tenure.

Her political career was inspired in part by Margaret Chase Smith, the Maine Republican who served in the Senate from 1949 to 1972. Ms. Collins once met Ms. Smith, who had delivered a famous denunciation of Joseph McCarthy, and noted that some constituents encouraged her to have a Smith-like moment of conscience when it came to Mr. Trump.

“I would argue that I have, like Margaret Chase Smith, taken a lot of tough votes and stood up for what I believe in,” she said. “But I think the best comparison is we each lost our last race for the Senate.

“I have now had my Margaret Chase Smith moment.”