The government has urged Whitehall bosses to "move quickly" to get more staff back into the office.
In a letter seen by the BBC, it says it is "strongly encouraging" attendance through rota systems, arguing this would be "hugely beneficial".
The government says it wants 80% of civil servants to be able to attend their usual workplace at least once a week by the end of the month.
But unions have described the government's attitude as outdated.
They said most civil servants should expect to keep working from home until the end of the year, and they would consider strike action if staff were forced to return when it was unsafe.
The letter applies to staff in England, with those elsewhere in the UK expected to follow local guidance and continue working from home.
It follows criticism that too few civil servants working from home because of coronavirus have returned to their desks, despite the easing of lockdown.
According to the latest data from the Office for National Statistics (ONS), there has been an increase in people travelling to work in the last two months, with fewer working exclusively from home.
They said 57% of working adults - out of 1,644 surveyed - reported that they had travelled to work at some point in the past seven days, while 20% had worked solely from home.
Thousands of businesses that rely on passing trade are suffering while offices stand empty, Dame Carolyn Fairbairn from the CBI has said.
But Alex Brazier, the Bank of England's executive director for financial stability, has warned that the government should not expect a "sharp return" to "dense office environments".
In the letter, sent to permanent secretaries - the highest officials in government departments - Cabinet Secretary Sir Mark Sedwill and Alex Chisholm, chief operating officer of the Civil Service, say that "getting more people back into work in a Covid-secure way will improve the public services we deliver".
They add: "We have seen a reduced level of social interaction among our colleagues, with the loss of some of the spontaneous interaction and cross-fertilisation between teams that drives innovation and sustained common purpose."
But they say staff safety "remains our paramount concern", and that workplace returns will be discussed with unions and staff groups.
Workplace guidance includes introducing one-way systems, staggered shift times and limiting the number of colleagues that staff members are exposed to in order to prevent the spread of the virus, such as only allowing a small number in lifts at any one time.
The letter goes on: "Departments which are still below their departmental constraints should now move quickly to seek to bring more staff back into the office in a Covid-secure way, and take advantage of the return to schools this month and increased public transport availability."
Prime Minister Boris Johnson has asked officials for a weekly update on progress.
Boris Johnson is clearly worried about the impact of empty office districts in major cities - and has been urging people to discuss going back to the office, where it's safe to do so.
Some Tory MPs want it to be the government's main priority now that schools are open again. They fear without movement soon, there could be extensive and lasting economic damage.
Encouraging civil servants back into the office could be seen as leading by example, perhaps showing how a system might work for other employers.
But unions warn the workplace has changed forever and ministers would be better focussing on how to adapt to a new working world.
The FDA union, which represents senior civil servants, said this week that it estimated 30% to 40% would be able to return to the office by the end of the year.
Leader Dave Penman accused ministers of "sounding like Luddites" in an era when technology made home working easier.
Mr Penman told BBC Radio 4's Today that one "fundamental problem" with the approach was that, on a practical level, government offices have a maximum capacity of around 50% because of coronavirus restrictions. He said the civil service was working "very effectively" from home.
He added it was "quite clear" that "this is really about virtue signalling to the private sector that has already moved on".
And Mark Serwotka, general secretary of the Public and Commercial Services Union, said he was prepared to consider industrial action "as a last resort" if workers' health and safety were "put at risk".
Meanwhile, outsourcing firm Capita - a major government contractor - is planning to close more than a third of its offices in the UK permanently.