Its Utrecht headquarters is in the former offices of Nederlandse Spoorwegen (known as De Inktpot, "The Inkwell"), the largest brick building in the Netherlands.

[2] Upon its creation, ProRail became responsible for the total cost of ownership and the long-term availability of the rail infrastructure, as well as to avoid operational safety being compromised.

[3][4] One early reform of the organisation, implemented for the 2007–2011 timeframe, was for all contracts to be publicly tender based on performance and process specifications.

[1] This was intended to facilitate effective competition to be awarded contract work while retaining the public service orientation sought by the government.

[1][5] In the late 2000s, in response to repeated year-on-year rises in both passenger and freight traffic on the network, ProRail developed a new 'Triple A' strategy to deliver a 50 percent increase in capacity, to be achieved via the adoption of smarter planning, the reorganisation of train services, and new construction works.

In late 2008, the Ministry of Transport allocated €4.5 billion for a multi-year investment to introduce the Triple A strategy along several key railway corridors.

[15] In 2014, the organisation released a report on various scenarios for rolling out the next generation European Rail Traffic Management System (ERTMS) across the Netherlands.

[17] During March 2022, ProRail announced that the French company Thales Group had been selected to provide signaling apparatus, referred to as the Central Safety System (CSS), in support of the ERTMS rollout.

[19] During June 2022, ProRail appealed to the Dutch government to subsidise train operators of both passenger and freight services, noting that its charges has to comply with the European rules for consumer compensation, yet the sector would suffer due to double digit price rises.

[20] In January 2023, figures released for 2022 showed that rail users had been subject to some of the worst performance statistics recorded in recent years in terms of delays and cancellations, which was in part attributable to strikes.

Funding for ProRail is primarily provided via a government subsidy, on top of which fees are charged to the various railway operators (called infraheffing).