Chancellor Rishi Sunak announced the awards as part of his package of measures to help the country to recover from the coronavirus pandemic.
Scarborough Council had applied for £25 million for each of Scarborough and Whitby from the Towns Fund but instead the two towns will share a pot of £37.3 million.
Scarborough is to get £20.2 million and Whitby £17.1 million.
In Scarborough these included:
* £6 million for a 16km Local Cycling And Walking Infrastructure Plan that would connect the town centre to Scarborough’s colleges and the Cinder Track.
* £5m for Scarborough Harbour regeneration
* £1.8m for interactive wildlife sculptures and hides.
* £1.4m to create a “FabLab+” in the town centre.
* £7m to overhaul the “gateway to Scarborough” from the train station with a new “public realm” and commercial properties.
In Whitby, projects previously announced included:
* £10m to build and set up the Whitby Maritime Academy.
* £2.6m for carbon neutral “self-build” homes for local residents.
* £3m to expand Pannett Art Gallery and Whitby Museum.
* £1m to improve the Grade II listed Town Hall and Market Square
* £750,000 to create a “Whitby Innovation Hub”.
* £2.3m to pedestrianise Whitby Swing Bridge.