The government has awarded £370,000 to the Royal Pavilion and Museums from the Culture Recovery Fund.
The trust that has been set up to run the venues is among more than 2,700 recipients of help from the £1.57 billion fund.
Brighton and Hove City Council said: “This award will enable the Royal Pavilion and our museums to reopen after lockdown, welcoming back visitors.”
The Royal Pavilion and Museums Trust chief executive Hedley Swain said: “This will make a major difference to our ability to reopen venues and do all we can to welcome as many visitors as possible in 2021.
“We are looking forward to welcoming visitors back safely and to continue to provide wonderful museum services for the people of Brighton and Hove and beyond.
“The Royal Pavilion and Museums Trust are incredibly grateful to Arts Council England, DCMS (The Department for Digital, Culture, Media and Sport) and Secretary of State Oliver Dowden for this vital grant.”
The council said: “The grant will help support the charitable trust as they reopen after the coronavirus pandemic.
“The lockdowns have severely affected the organisation which will still face a very difficult year financially in 2021.
“The trust plans to reopen the Royal Pavilion and the four other venues with a range of cultural activities to attract the many visitors expected to flock to the city this summer.
“This will include the opportunity to see A Prince’s Treasure at the Royal Pavilion which reopens on Monday 17 May with spectacular items on loan from Her Majesty the Queen in their original setting. The exhibition has been extended until January 2022.
“The hugely popular photographic show of David Bowie – Rock n Roll with Me: Bowie/MacCormack 1973-76 has also been extended until January 2022.
“This show sold out during the short window when the museum could open in the autumn and is expected to be hugely popular this summer.
“Tickets go on sale on Wednesday 9 April and the museum reopens on Tuesday 18 May.
“Preston Manor will reopen on Friday 28 May with new family trails to provide entertainment for local residents during the school holidays and for tourists, many who are expected to visit from the UK this year.”
The Royal Pavilion and Museums Trust’s chair of trustees Michael Bedingfield said: “Culture is an essential part of the Brighton and Hove economy and will be essential to its recovery after such a difficult year.
“As an organisation we want to play our full part to attract visitors back to our wonderful city and to enjoy all it has to offer.
“Our fantastic museums and the world-famous Royal Pavilion are great attractions for local residents and people from all over the UK and the world.
“However, 2021 will continue to be very difficult and unpredictable for our organisation. We will continue to need lots of support from our stakeholders, supporters and audiences.
“This could be visiting one or all of our venues when they reopen, visiting our fantastic Royal Pavilion shop or donating to our charitable fund.”
Last summer councillors agreed measures to help the trust. It looks likely to be given financial help worth more than £1.5 million and to be able to draw money from a £4 million council-backed “cash flow facility”.
The council and trust had previously agreed a £500,000 cash flow facility which would operate like a bank overdraft – to provide a “financial safety net”.