The Prairie Dog Central Railway  began operations in regular public service on July 11, 1970.  From 1970 – 1974, the train operated out of Charleswood along Wilkes Boulevard on the former Canadian National Cabot Subdivision.  From 1975 to 1996 the train then operated out of St. James and the old St James Station, immediately west of Polo Park on the Canadian National Oak Point Subdivision and ran to Grosse Isle and back.

In 1996 the Society was advised by CN that the Oak Point Subdivision was to be abandoned and in addition to that, the Transcona shops (where the train was stored and maintained) could no longer support the Prairie Dog Central Railway operations.  Consequently, soon after 1996 the Prairie Dog Central Railway ceased its train operations for two seasons and the Society embarked on a major fundraising campaign and raised $1.3 million dollars to purchase the Oak Point Subdivision. The St. James Station had now been declared a Heritage Building by Parks Canada. Under special approval the Station was relocated to its current location at Inkster Boulevard and Sturgeon Road along Prairie Dog Trail. Operations began shortly thereafter travelling from Inkster Junction Station to the Manitoba communities of Grosse Isle and Warren for a stop-over, before heading back to Inkster Junction Station.