Originally opened on April 28, 1940, the network consists of 15 routes, with 174 trolleybuses operating on 68 miles (109 km) of two-way parallel overhead lines.

[3] As of the third quarter of 2024, the system carries riders on an average of 39,500 trips per weekday,[8] comprising about 18 percent of King County Metro's total daily ridership.

The demonstration was a success, but still reeling from the impacts of the Great Depression, Seattle voters rejected the plan in a municipal election on March 9, 1937.

[10][11] In 1939, Seattle received a federal loan that allowed the city to retire the debts from the streetcar and cable car system.

The city's aging trolleybuses were spiffed up, and the overhead wire expanded in 1962 to serve the World's Fair, but citywide the Seattle Transit System was increasingly abandoning the trolley routes.

That study contradicted the claims of management, concluding that trolleybuses perform better than diesel powered buses on Seattle's hills and that operating costs were comparable (except for overhead wire maintenance).

[5] There had been "prolonged and vocal [public] opposition to the 1970 conversions"[15] of routes 3 and 4 to motor buses, leading city officials to begin working to ensure that the system would survive under Metro.

[15] Furthermore, the city was interested in expanding the system, in light of the fuel shortages and price increases observed during the 1973 oil crisis, and in 1974 it formally asked Metro[5] to add 27.5 route mile and up to 63 vehicles.

[15] The proposed expansion was later scaled-back slightly, but the final plan agreed to by the City and Metro would eventually see the system expand from 55 vehicles to 109 and from 32 route miles to 55[5] by 1981, in addition to replacement of all of the old fleet and infrastructure with new.

These were the first articulated trolleybuses in North America, other than single experimental vehicles or manufacturer demonstrators on loan,[27] and they began to enter service in April 1987.

[14] In September 1997, King County Metro expanded the trolleybus system, electrifying Route 70 between downtown and the University District via Eastlake Avenue E.[14] The $19 million project, primarily funded by a grant from the Federal Transit Administration, was the first modern expansion of trolley wire (excluding the downtown bus tunnel) and incorporated public art as required by city ordinances.

As part of an effort to cut costs across the agency, a 2009 King County Auditor's Office report recommended replacing the trolleybuses with hybrid diesel-electric coaches.

[34] Facing a situation similar to the 1970s and pressure from the public, King County Metro commissioned an independent evaluation of the trolleybus system.

[32] The Xcelsior XT40 and XT60 are the first trolleybuses in King County Metro's fleet to have a low-floor design, a wheelchair ramp (instead of a lift), air conditioning and an auxiliary power unit (that allow buses to operate off-wire for at least 3 miles).

After years of planning, King County Metro installed a new section of trolley wire near Seattle Pacific University in North Queen Anne and placed it into service in March 2017.

As part of a project to improve the arterial, SDOT is adding new, stronger streetlight poles that will be capable of supporting the weight of trolley wire.

[53] SDOT has also identified several possible future trolley wire expansions in its Transit Master Plan, including two key projects: electrifying Denny Way between Uptown and Olive Way (which would allow a portion of busy Route 8 to operate with trolleybuses) and electrifying Yesler between 2nd and 9th Avenues, and on 9th Avenue from Yesler to Jefferson (which would allow Routes 3 and 4 to travel on a less congested path between Downtown and Harborview Medical Center).

The steepest grade on the system is 19 percent in the block of Madison Street between 3rd and 4th Avenues in downtown, where traffic runs in the downhill direction only.

The new trolleybuses are built with motors from Škoda[35] and a Vossloh Kiepe electric drive system, including an auxiliary power unit (lithium ion phosphate batteries)[35] that allow buses to operate off-wire for at least 3 miles, a first for Metro.

Strong ridership growth during World War II, when the city's economy was booming, brought a need for additional vehicles.

[15] Not long afterward, a shortage of serviceable vehicles prompted Metro Transit to re-acquire four trolleybuses that previously had been donated to museums.

Metro immediately repainted it into its original Seattle Transit System paint scheme only used during the 1940s, and it returned to regular service in November 1975.

[16] With electrification of motor bus routes 15 and 18 planned, in 1984 Metro placed an order with MAN, of Germany, for 46 articulated (bending) trolleybuses.

[28] The planned conversion of routes 15 and 18 to trolleybuses was later deferred, as funds needed to be diverted to the downtown tunnel project, and was ultimately canceled.

Metro borrowed a prototype Renault articulated, dual-mode bus from its French manufacturer in 1982–1983 to evaluate the technology and gain experience with it.

Metro ultimately awarded a contract for an order of 236 dual-mode buses to Breda Costruzioni Ferroviarie in October 1986, at a cost of $133 million,[67] subsequently approved by the federal government's UMTA in November.

However, additional studies and strong public opposition to the proposal ultimately resulted in Metro's decision to purchase another fleet of new trolleybuses to replace the old vehicles.

The prototype XT60 articulated unit was received by Metro on June 1, 2015, and the production-series vehicles began arriving in December 2015, with the first day of service for the type being January 29, 2016.

[80] The Metro Employees Historic Vehicle Association (MEHVA) has preserved and restored several vintage trolleybuses from the system's past fleet.

[60] When the system reopened in 1979 after its almost-two-years shutdown for rebuilding, Jefferson Base remained Metro's sole trolleybus garage, but a move back to Atlantic was planned.