Phase I of the system, operating on an existing right-of-way from Belen to Bernalillo that NMDOT purchased from BNSF Railway, opened in July 2006.

Later that same year, grants were given to NMDOT and MRCOG to begin the effort, and the New Mexico State Legislature passed Governor Richardson's Investment Partnership (GRIP), a transportation improvement package with the Rail Runner included as one of the bill's projects.

Over the next few years, NMDOT and the Mid-Region Council of Governments (MRCOG) developed a strategy for implementing the rail service.

After assessing the needs of the track, the state of New Mexico committed to purchasing the railroad corridor from Belen to the New Mexico-Colorado border from BNSF (although, thus far only the portion between Belen and Lamy, NM has been purchased)[citation needed], to ensure that commuter trains would always get the right-of-way and have priority over freight trains in the corridor.

[4] The Rail Runner officially went into service on July 14, 2006, serving the Downtown Albuquerque, Los Ranchos, and Sandoval County stations.

Using the existing Santa Fe Southern Railway track from Lamy to Santa Fe, which is filled with sharp curves, would have required the train to slow to 15 miles per hour (24 km/h) in some places, so new tracks were laid to allow travel times comparable to the automobile.

The route uses previously existing track from Bernalillo to the base of La Bajada, a hill south of Santa Fe.

Officers are charged with protecting the trains, inspecting fares, and addressing issues at the stations and parking lots.

During the suspension, Rio Metro continued to run empty trains along the route in order to maintain readiness of the vehicles and crew.

Citing the high cost of gas, Governor Michelle Lujan Grisham announced in July that the reduced fares would be extended until the end of 2022.

In addition, two round trips would be added on August 1 as part of a revised schedule focused on all-day frequency rather than traditional commuter service.

[19] In late 2007, the Rail Runner was the subject of more criticism as a transportation funding shortfall left many state road projects stalled.

Two separate gross receipts taxes for regional transit were approved by voters in central and north-central New Mexico in November 2008 to cover a large portion of the operational funds of the Rail Runner.

In November 2006, free service ended on the line's Sandoval section, and ridership fell to 1,000 passengers per day.

When the Los Lunas and Belen stations opened with free service, ridership rose to around 1,800 passengers per day.

Free service on the Belen section of the line ended April 1, 2007, and a new zone fare structure went into effect.

The original 2005 projected ridership for a slightly different (but similar speed) Phase II route to Santa Fe was 2,954 daily riders.

After a cumulative total of 227 passengers made use of Lobo, the game-day train service was discontinued and the station abandoned.

Additional service is provided for some events like the New Mexico Wine Festival; connecting bus shuttles run for the Balloon Fiesta.

The "door closing" tones resemble the signature “Beep-Beep” of the Warner Bros. Road Runner cartoon character.