The system consists of a single, 6.4-mile-long (10.3 km) light rail line that runs for most of the length of Main Street (New York State Route 5) from KeyBank Center in Canalside to the south campus of the University at Buffalo in the northeast corner of the city.

[5] Despite the decline of Buffalo's industry and population over the next few decades, federal funds and a desire to revitalize downtown spurred the Niagara Frontier Transportation Authority, the IRC's successor, to construct the modern Metro Rail line, starting in 1979.

It came amid a surge in light rail construction in mid-sized cities nationwide, as Denver, Portland, Sacramento, and San Jose also built systems at the same time.

The cost of the urban section was so high that no funding was available to extend the lines into the suburbs, including the Amherst campus of the University at Buffalo.

[10] The project in question involved creating a shared trackbed/roadway with curbside parking, as well as the permanent closure of the Theater Station, which occurred on February 18, 2013.

The project is being constructed in conjunction with the total replacement of the trackbed in the 400 block as well as the installation of a crossover track to decrease the effects of single-tracking during the process.

[14] In 2019 Tim Kennedy and Crystal People-Stokes secured a $100M state commitment to fund renovation and repair work throughout the system that had largely been delayed since the line's opening.

[18][20] The Buffalo trains join Philadelphia's SEPTA light rail cars as the only modern non-articulated LRVs operating in the United States.

[23] Metro Rail runs as follows: Monday-Friday from 5:10 am-12:50 am, Saturdays from 7:05 am-12:50 am and Sundays and holidays from 8:00 am-11:50 pm (although most bus service is available until approximately 12:30 am).

"[24] As a result, the following September, the NFTA implemented an earlier start for the weekday schedule in response to an 11% increase in ridership over eight months of growth.

However, it is noted that the line currently lacks extended branches to the suburbs, being confined to the city limits of Buffalo.

In April 2011, the group stated that the 600 block of Main Street, which has Shea's Performing Arts Center along with hotels and bars, should be converted into a mixed automobile and rail system.

In December 2012, the NFTA announced it had secured funding of $1.6 million to commission a study in 2013 of bus and rail access to University at Buffalo's North Campus.

The light rail corridor would extend from a turnout at University station, head north to Niagara Falls Boulevard past the Boulevard Mall, turn to Sweet Home Road, enter the University at Buffalo North Campus and parallel Interstate 990 ending at the Crosspoint Business Park in Getzville.

[29] Planning and funding is currently underway for a northbound Niagara Falls Boulevard extension to the University at Buffalo North Campus.

In addition, the chosen corridor would parallel Audubon Boulevard and end at a park-and-ride after passing under I-990, rather than continuing to the Crosspoint Business Park.

[33][34] The Airport corridor would begin in Downtown Buffalo, near Church station and continue in an easterly direction in/out Division Streets, diagonally in a northeastern direction near Jefferson Avenue toward the Buffalo Central Terminal, cross Broadway and then continue eastbound in its private right-of-way to the Thruway Plaza, Walden Galleria and Buffalo-Niagara International Airport.

It was determined after initial trial runs that the PCCs were too wide for existing station platforms and the plan was abandoned.

The NFTA has a fleet of 27 (originally 29) rigid-bodied (non-articulated) LRVs for the Metro Rail system, numbered sequentially from 101 to 127.

The NFTA acquired twelve PCC streetcars from the Greater Cleveland Regional Transit Authority in 1990 for service on the never-built Tonawandas branch.

[48] After a lengthy delay, which put the project years behind the original schedule, the first two cars (fleet numbers 114 and 123) were returned to service on March 9, 2012.