Buses and light rail services will receive £283m towards improving safety and restoring services during the coronavirus pandemic.
However, Transport Secretary Grant Shapps said the full service would only run at a fifth of the usual capacity because of social distancing rules.
Announcing the funding, he said it does not mean "we can go back to using public transport whenever we like".
Volunteers will also be used to double the 3,400 safety marshals at stations.
The £254m for buses and £29m for trams and light rail is intended to increase the frequency and capacity so the UK can "start moving back to a full timetable", Mr Shapps told the Downing Street daily briefing.
But he added: "Only if you need to travel and you can't cycle, walk or drive should you take the bus, tram or train."
People who can work from home should continue to, he said, and those travelling by public transport for essential purposes should "please avoid the rush hour".
The funding is expected to enable adjustments to vehicles, signage, deep cleaning and the provision of hand sanitiser.
From 1 June, Mr Shapps said the government would also bring in more marshals at stations to join the 3,400 British Transport Police officers, Network Rail and train operator staff currently advising passengers and monitoring social distancing.
He called these new volunteers "Journey Makers", and said they reflected the same "public-spirited concern" as the volunteer Games Makers at the London 2012 Olympics.
'Build them fast'
Suggesting that the government wants the UK to come out of the coronavirus crisis stronger "by permanently changing the way we use transport", he said it was working on plans to allow people to park outside of city centres and finish their journey on bike or on foot.
Development funding for 10 new projects was also announced as part of the government's plan to reverse some of the 1960s Beeching cuts to local railway services.
They include the "Ivanhoe line" from Leicester to Burton-on-Trent, branch lines on the Isle of Wight and a new station at Wellington in Somerset.
He said if the plans are viable, "we're going to build them fast".