Rishi Sunak’s relief that Nadine Dorries is finally standing down as an MP has been tempered by fears of a difficult byelection ahead and anger among Conservative backbenchers that her angry outbursts will end up on Labour’s general election leaflets.

The former cabinet minister and Boris Johnson loyalist resigned her Commons seat of Mid Bedfordshire on Saturday, accusing the prime minister of betraying Tory principles and telling him: “History will not judge you kindly.”

Her resignation means the government faces yet another challenging contest this autumn in what should be an ultra-safe seat. If Labour can overturn the 24,664 majority, it would represent the largest collapse in support for the Conservatives in byelection history.

The explosive manner of Dorries’ departure has angered soon-to-be former colleagues, with the senior Tory MP Tobias Ellwood describing it as an “undignified chapter” and “an episode of colleagues throwing their teddies in the corner, in this case for simply not getting a peerage”.

He told GB News: “It has been messy, it has been embarrassing for both the parliament and specifically to our party. Delaying this resignation was designed to maximise harm to the prime minister. I’m pleased that this sort of selfish charade is now over.”

One Tory backbencher told the Guardian: “Nadine has done the party a great disservice by attacking Rishi in such a way. Her words will end up on every Labour party leaflet at the next election.”

The defence minister Johnny Mercer said people were not interested in hearing Dorries’ latest “personal attack” on Sunak, and the party needed to move forward having “raked over the coals of the Boris Johnson premiership a number of times”.

Government insiders said Sunak was determined to press ahead with plans for the autumn attempting to show people struggling with the cost of living that a better future lies ahead.

However, with inflation expected to tilt upwards again next month as the Tories gather for their party conference, Sunak could struggle to convince voters that the economy is back on track.

The prime minister faces continued grumbles from backbench MPs who want the government to cut taxes. Meanwhile, in the government’s final themed policy week before parliament returns next Monday, ministers are making a series of announcements on policing and the criminal justice system.

The Conservatives are still reeling from the loss to Labour of Selby and Ainsty, in North Yorkshire, in a byelection this summer when Keir Starmer’s party overturned a majority of just over 20,000.

Labour believes it is best placed to gain Dorries’ traditionally safe Tory seat, having come second in 2019. The party’s chair, Anneliese Dodds, has conceded it would “take an absolutely enormous change” for Labour to win.

The Lib Dems, who came third in 2019, have also said they could win, having achieved massive swings to take similar rural so-called “blue wall” seats where Conservative support has traditionally been strong.

The Tories’ challenge in defending Mid Bedfordshire could be compounded by local voters’ evident frustration over Dorries’ absenteeism in representing the constituency. She had not spoken in the Commons since June 2022 and last voted in April.

The divisive circumstances of her exit, after she delayed her departure to investigate why she had been refused a seat in the Lords, may also not help.

In her scathing resignation letter to Sunak, Dorries wrote: “Your actions have left some 200 or more of my MP colleagues to face an electoral tsunami and the loss of their livelihoods, because in your impatience to become prime minister you put your personal ambition above the stability of the country and our economy.

“Bewildered, we look in vain for the grand political vision for the people of this great country to hold on to, that would make all this disruption and subsequent inertia worthwhile, and we find absolutely nothing.”

A byelection writ cannot be moved until parliament returns next month, so the contest will not be held until October at the earliest.