MI5 intelligence will be shared with bodies outside the security community in a drive to stop terror suspects before attack plots can crystallise.
Ministers will also bring forward strengthened anti-terror laws to allow earlier interventions, and target the "insider threat" at airports amid warnings the aviation system remains a "totemic" target.
Details of the measures emerged as the Government unveiled its new blueprint for tackling terror.
In a major shift, MI5 will declassify information on individuals who have appeared on its radar - but are not currently under active investigation.
Details could be passed to bodies such as councils, local police or government departments, who will work alongside intelligence agencies to determine the best course of action to manage the risk.
Greater intelligence-sharing is seen as necessary to minimise the threat posed by suspects who are rapidly radicalised to the point of violence before security services can detect the shift.
Salman Abedi, the Manchester bomber, was categorised as a "closed subject of interest" at the time of the attack, and so not under active investigation.
There are an estimated 20,000 individuals who have previously featured in terrorism probes, either as active targets or on the periphery of inquiries.
Officials emphasised that the new project will be on a much smaller scale - with the number of cases where intelligence could be shared expected to be in the low hundreds over the next year.
The new "Contest" strategy document, published on Monday, says: "We will share information more widely and support more local interventions with individuals in our own communities who are being groomed or incited to commit or support acts of terrorism."
New "multi-agency approaches" will be rolled out, initially in London, the West Midlands and Greater Manchester.
The paper adds: "By alerting a greater number of agencies to individuals of potential concern, we will improve our ability to assess the risk they pose whilst also being able to bring to bear a broader, larger set of local interventions."
Theresa May said the new strategy "has a much greater focus on systemic co-ordination across the public sector".
The Prime Minister added: "By linking up not just the intelligence agencies but also local authorities, health providers and many others, it will make it harder than ever for terrorists and those who support them to plan and carry out attacks."
A huge exercise was launched across Government, intelligence agencies and policing to identify new measures to stop atrocities after five attacks hit the UK in less than six months in 2017.
The refreshed strategy, which is the fourth published version of Contest and the first update since 2011, outlines the need for a "step change" in investigative capabilities. It also:
- Commits to new anti-terror legislation aimed at boosting powers available to police and prosecutors so they can intervene at an earlier stage in investigations.
- Warns that the global aviation system remains a "totemic" target for terrorists and highlights the need to target the "insider threat" by strengthening information-sharing about those working in sensitive environments in airports.
- Sets out plans for longer prison sentences for some terror-related crimes and strengthened management of offenders after they are released.
- Details how 900 individuals "of national security concern" have travelled from the UK to engage with the Syrian conflict, with 40% having returned.
- Calls for closer ties with the private sector to speed up alerts about suspicious purchases and eradicate online "safe spaces" for terrorists.
- States that MI5 will have a greater role in the assessment and investigation of extreme right-wing terrorism.
Since March last year, 12 Islamist and four extreme right-wing attack plots have been foiled.
MI5 and police are running more than 500 live operations involving roughly 3,000 active "subjects of interest" at any one time.