The Pfizer/BioNTech vaccine will be used as the booster dose for around 30 million people, with experts saying it is safe to be given alongside the usual winter flu jab.
People will be able to get their Covid and flu vaccines on the same day, preferably with one shot in each arm.
Health Secretary Sajid Javid told the Commons that the NHS would contact all those who are eligible and was preparing to offer the jabs from next week.
Wales has also said it will begin a rollout of booster vaccines. Updates are expected from Scotland and Northern Ireland later on Tuesday.
All those who are clinically extremely vulnerable and anyone aged 16 to 65 in an at-risk group for Covid (who were included in priority groups one to nine during the initial vaccine rollout) will also be eligible for a jab.
Three vaccines have been approved as safe and effective as boosters - AstraZeneca, Pfizer and Moderna - but experts have decided to opt for Pfizer as a preference after studies showed it is well tolerated and works well as a booster.
It can be given to people who had two doses of AstraZeneca previously.
Moderna may be used as an alternative, but as a half-dose booster shot after studies showed it was effective, with few side-effects.
People should receive their third booster dose at least six months after they received their second dose of a Covid vaccine.
When there is more data, experts from the Joint Committee on Vaccination and Immunisation (JCVI), who prepared the advice to ministers, plan to look at whether boosters should also be offered to healthy people under the age of 50.
Professor Wei Shen Lim, chairman of Covid-19 immunisation for the JCVI, said: "The UK's Covid-19 vaccination programme has been hugely successful in protecting people against hospitalisation and death, and the main aim of the booster programme is to prolong that protection and reduce serious disease as we head towards the colder months.
"The JCVI is advising that a booster dose be offered to the more vulnerable, to maximise individual protection ahead of an unpredictable winter.
"Most of these people will also be eligible for the annual flu vaccine and we strongly advise them to take up this offer as well."
The new guidance from the JCVI appears to differ to its interim guidance published in June.
The interim guidance said anyone over 16 who qualifies for a seasonal flu jab would be included in the booster campaign, which would have included millions of people with asthma.
This has been scrapped, and only those in original priority groups one to nine will be offered a booster, meaning not all those with asthma may be included.
Professor Jonathan Van-Tam, deputy chief medical officer for England, told a Downing Street briefing: "We know that this pandemic is still active, we are not past the pandemic, we are in an active phase still.
"We know this winter could be bumpy at times and we know that winter viruses such as flu and RSV (respiratory syncytial virus) are highly likely to make their returns.
"So with that in mind, the aim of the game - the mantra - is to stay on top of things."
Prof Van-Tam said that if he was offered the flu jab and a Covid-19 booster at the same time, he would take it.
Mr Javid added: "Almost six million people over the age of 16 remain unvaccinated in the UK, and the more people that are unvaccinated the larger the holes in our collective defences."
On booster doses he said: "There's evidence that the protection offered by Covid-19 vaccines reduces over time, particularly older people who are at greater risk, so booster doses are an important way of keeping the virus under control for the long-term."
He added: "They (JCVI) recommended that people who were vaccinated in Phase 1, that is priority groups one to nine, should be offered a booster vaccine, that this vaccine should be offered no earlier than six months after the completion of the primary vaccine course and that as far as possible the booster programme should be deployed in the same order as Phase 1."
"I can confirm that I have accepted the JCVI's advice and that the NHS is preparing to offer booster doses from next week."