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For three decades, Susan Collins has styled herself as a moderate conservative who delivers for Maine, even when it means defying Donald Trump. But as the incumbent Republican seeks a sixth term, national Democrats see her as newly vulnerable – zoning in on the state as a clear path to reclaiming the Senate.

Collins, 73, will now face off against the presumptive Democratic nominee, Graham Platner, a 41-year-old marine veteran and oysterman with no national political experience and a controversial past. Despite dredged-up racist, sexist and homophobic online posts – and a now-covered-up tattoo that resembled a Nazi symbol – Platner continues to amass a rare kinetic energy that has seen hundreds of Mainers flock to town halls across the state to hear his gravelly voiced excoriation of Washington. His rise ultimately forced the state’s two-term governor Janet Mills to suspend her primary bid, citing dwindling financial resources.

Platner’s youth and outsider profile have created a sense that Maine – a state with the oldest and whitest population in the country – may be ready for a change in political leadership. There’s a prevailing sense of “we like her, and she’s been good for Maine, but she’s had her time for somebody new or younger”, one former state Republican official, granted anonymity to speak candidly about the race, said of Collins. The senator’s campaign spokesperson did not respond to the Guardian’s request for comment about her performance to date.

The other man causing problems for Collins this midterm election is the president himself. The Pine Tree state is one of four seats that Democrats see as a viable pick-up to regain control of the upper chamber come November. Collins is the only Senate Republican running for re-election in a state that Kamala Harris won in 2024, and this will be the first time she is back on the ballot since Trump’s return to the White House last year – ensuring a nationalized contest shaped by foreign‑policy crises, high gas prices, persistent inflation and a domestic agenda defined by a sweeping immigration crackdown, deep Medicaid cuts and weakened federal agencies.

In the past, Collins has been unafraid to defy Trump directly. She voted to convict the president during his second impeachment trial after the January 6 insurrection, opposed Pete Hegseth’s nomination for defense secretary, and voted to confirm liberal supreme court justice Ketanji Brown Jackson. But she has also backed many of the president’s priorities. Her vote to confirm Brett Kavanaugh, and the Dobbs decision that followed, still looms large. So does her support for a national voter‑ID bill and her delayed backing of a war‑powers resolution on Iran. It didn’t help when Democrats seized on an image of Collins holding a Maga cap in the Oval Office earlier this year.

Her maneuvering on Capitol Hill has the potential to cast her as more of a background actor, as opposed to a key player this cycle. “She is the most talented Senate staffer to have a seat in the Senate,” said Tony Payne, a former executive director of the Maine Republican party. “The feeling is widespread that she will show her independence only when her vote is not required.”

Platner has leaned hard into that critique, branding Collins’s moderation as complicity. In a recent ad, he called her breaks with Trump “symbolic opposition” that don’t “reopen hospitals” or “bring back Roe v Wade”, and accused her of selling out working‑class Mainers to the president and the “Epstein class”.

Trump, meanwhile, has no viable Republican alternative to Collins. Unlike in Louisiana or Kentucky, there is no hardliner he can throw his weight behind with a retributive, all-caps endorsement on Truth Social. After years attacking Collins – as recently as January he said she “should never be elected to office again” – the president has shifted to faint praise, calling her a “good person” and hoping she wins. While his blessing is a vital currency in deep-red pockets of the country, in Maine it could be a liability, particularly among libertarian‑leaning voters wary of the Republican party’s Maga wing.

“She really needs silence from [Trump], and he’s not good at that,” said Jeffrey Selinger, professor of government at Bowdoin College. “She has to not poke the bear, but then still claim credit for things that she thinks she did well.”

While speaking in Bangor last week, JD Vance even offered a veiled acknowledgement of Collins’s predicament. “The thing I love about Susan is she is independent because Maine is an independent state,” the vice-president said. “And frankly, if she was as partisan as I sometimes wish that she was, she would not be a good fit for the people of Maine.”

In early matchups, Collins trails Platnerby single digits, but she has survived poor polling before. Collins also has money on her side: the top Senate GOP Super Pac has invested $42m in the race, with more outside spending pouring in. Republicans will now have ample runway and the deep pockets to discredit Platner, especially by resurfacing the controversies that beleaguered the early months of his campaign. Political operatives in the state also said that more opposition research will likely flood the race in the lead-up to the election.

While Platner is running a “top shelf” campaign, with impressive media, Maine rewards old‑style politics, according to Lance Dutson, a GOP strategist who has worked on Collins’s previous campaigns.

And at the Maine Republican convention last month, Collins made her case clear to members of her party gathered in Augusta. “I’m going to be talking about my record of delivering for my beloved state,” she said, vowing to highlight her seniority as chair of the powerful Senate appropriations committee, and the influence she’s built over nearly 30 years in the Senate. In her first general election spot, Collins followed through, focusing on the federal funding she secured to repair a collapsed pier in Eastport, instead of slamming her opponent.

Her tenure as a camera-shy workhorse could also outweigh any “abstractions around her character”, Dutson added. “If I’m in a town of 1,500 people and Susan Collins got us the new fire truck, that’s more impactful than her opinion of Trump.”