The money comes less than a month after the council accepted a grant of more than £800,000 from the same body's Museums Estates Development Fund (MEND) towards essential repair work to the outside of the city's flagship building.
The latest award will fund a project to give the museum the ability to host "larger scale and more complex exhibitions."
The historic venue closed its doors in October for three years of renovations in a £10.7m "Re-imagining the Harris" project aimed at creating the nation's first "blended" museum, art gallery and public library.
The city council wants to make the Grade I Listed building more accessible and at the same time show off its architectural splendour.
The latest Arts Council England grant, which comes on top of the main project, will allow a complete overhaul of the Harris’s three special exhibition galleries.
The work will see a partitioned area on the second floor brought back into use after three decades.
The total cost of the special exhibition gallery scheme is £653,900, with 10 per cent - £68,900 - being footed by the council itself from its £1.9m Town Fund budget.
A report to councillors about the funding from the Arts Council England's Capital Investment Programme (CIP) says: "The fund is an open access programme to support cultural organisations to adjust buildings and equipment so that they can operate safely post-pandemic and improve access, size on technological opportunities and reduce environmental impact.
"The CIP will allow the Harris to upgrade the special exhibition galleries to government indemnity standard, providing the ability to host larger scale and more complex exhibitions."
It follows the £803,249 grant handed to the council by Arts Council England's Museums Estates Development Fund which the city council applied for last October.
That funding, which will also be backed up with a 10 per cent (£89,250) contribution from the city council.
The overall Re-imagining the Harris project is set to "deliver a significant range of benefits to Preston."
"The Harris will support cultural tourism for the city through a significant programme of events," says a council report.
"This is a transformational project and one that will play a significant part in the growth of the city."