Worth £100,000 annually over four years, the fund will provide up to half of project costs.
The scheme aims to allow councils and community organisations to deliver projects which contribute to its vision of providing a “doorstep to destination” journey for customers, whilst reducing congestion and pollution.
Individual projects could include improving directions and signs for cyclists to and from stations, and upgrading connections between stations and other local services such as schools and town centres.
It could also help to fund new facilities for customers travelling to stations by bike.
ScotRail Alliance cycling manager Kathryn Mackay said: “We’ve delivered an unprecedented investment in cycling in recent years, with the provision of Bike and Go at 12 stations, and over 1,200 extra cycle spaces.
“We are encouraging councils and local community groups to take advantage of this great opportunity. It’s all part of our plan to build the best railway Scotland has ever had.”