The Ripon Museum Trust will be awarded £560,000 over the next four years by the Arts Council England.
The culmination of years of hard work and dedication from the Trust's volunteers, trustees and leadership team, the city's Workhouse Museum and Garden, the Courthouse Museum, and the Prison and Police Museum, will all be added to the council's National Portfolio, which will drive forward a series of major projects.
The Director of Ripon Museum Trust James Etherington said: "There are things that we have dreamed of for a very long time and things we said we would do if only we had more resources.
"Now we have it all in one swoop, we are very excited."
The funding will enable the Trust to commission a new art work every year for four years, after the success of the Workhouse's Consumption project by artist Pippa Hale - a day-long filmed performance of over 50 volunteers taking part in the recreation of a workhouse meal in 1861.
The courthouse museum will be the first focus of the art commissioning.
The £560,000 will also help the museums to continue to strengthen links with the wider community.
Learning Manager Carrie Philip said: "We are very excited about the funding. It will allow us to engage with more schools and share more of our wonderful stories from the museums."
Volunteers Manager Wendy Hunwick-Brown, said: "The funding is about taking our museums out to different audiences and as many different people as possible.
"We want to explore more digital ways of telling our stories and bringing those stories to life.
"We would love to reach out more to people who wouldn't normally necessarily visit museums. It would be great to get more young people involved.
"We are all absolutely thrilled to have been awarded the funding, it wouldn't have been possible without our team of amazing volunteers."
The Chair of Trustees, Richard Taylor, said: "I feel that it is a coming of age for the Ripon Museums Trust.
"We are thrilled to be recognised by Arts Council England as an organisation worthy of National Portfolio status.
"It gives us the chance to plan our future with more certainty."
A statement from the Arts Council said: ""Ripon Museums Trust is an outstanding example of a volunteer led museum which works at the heart of its rural community."
The national recognition of the museums as a vital community resource and tourist attraction also helped to secure a £402,400 Heritage Lottery Fund grant to expand the workhouse and open the main block.
The expansion will open up to visitors the original Master's wing, dormitories, the main dining room which also doubled up as a chapel, and the male and female yards.
The first section of the main block opens on July 19.