Bus and train services to and from the golf resort will also be stepped up during the tournament as organisers seek to avoid traffic congestion.
All spectators will have to arrive by a dedicated bus or train, with no access for private vehicles during the event, which runs from September 23 to 28.
Access to Gleneagles rail station is being enhanced, and a temporary footbridge will carry ScotRail passengers over the A9.
Two new temporary bus terminals are also being constructed to handle the flow of park-and-ride buses. Access to and from the nearby town of Auchterarder will be kept open, but road restrictions will apply.
Locals are being informed of the proposed transport plan at a series of meetings taking place in Auchterarder, Kinross, Stirling and Perth this week.
The three park-and-ride facilities at Balado in Perth and Kinross, Perth and Stirling are expected to cater for the majority of the thousands of golf fans attending. Balado, which is well known as the home of the T in the Park music festival, is just over 16 miles away. Perth and Stirling are even further afield.
Antonia Beggs, operations director at Ryder Cup Europe, said: "Our transport plans for the 2014 Ryder Cup aim to ensure that people can get on with their daily lives, while also help delivering one of the greatest sporting events in the world.
"We have tried to ensure that the event is as sustainable, safe and efficient as possible."
Laurence Kenney, from Transport Scotland, said: "Partnership has been key to the detailed planning undertaken to develop this transport plan which aims to ensure the reliable transport of thousands of spectators, while also keeping Scotland's major roads flowing. The three park-and-ride facilities, combined with enhanced rail provision, offer a number of options for spectators, while also minimising the impact on local communities."
He added that recent investment in upgrading Gleneagles station and the creation of an expanded park and ride at Stirling will encourage greater use of public transport. Mr Kenney said the facilities would leave a lasting legacy for local communities.
Ian Miller, leader of Perth and Kinross Council, said: "We want all spectators to enjoy their visit to Gleneagles.
"We are confident the transport plan will help to deliver this, while ensuring the majority of local people can continue with their daily lives as normal."
The park and rides will each have dedicated provision for cyclists, and pedestrians will be prevented access due to safety. There will be drop-off facilities at all park and rides for taxis and private vehicles.
It is estimated the tournament will benefit the Scottish economy by about £100 million.
The event is being held on Scottish soil for the first time in almost 40 years.