The first phase of the system, a 43-mile (69 km) segment between Northern Santa Rosa and downtown San Rafael, opened to public preview and excursion services (as far south as Marin County Civic Center) on June 29, 2017.

[5] Regular service began on August 25, 2017, after the Federal Railroad Administration (FRA) gave the final approval for the positive train control (PTC) system.

The last passenger rail service along the Northwestern Pacific Railroad south of Willits was discontinued in 1958 as automobile travel along U.S. Route 101 in California increased in popularity.

[7] Previously disused station buildings were repaired in anticipation of reestablished rail service in Healdsburg and Windsor, and Cloverdale's depot was constructed in 1998.

[9] The recommended remedies, which were certified without challenge, included silencing of some train horns in quiet zones[10] and replacement of certain wetland ditches.

According to SMART General Manager Farhad Mansourian, “This will not only address the 2.2 acres (8,900 m2) of project impacts that were determined through the environmental review process for the next stage of construction, but ensures a local source for potential future mitigation needs for the rail and pathway project.”[11] The project is funded by federal, state, regional and local allocations including bridge tolls, dedicated sales tax revenues, and fares.

[citation needed] However, the economic downturn reduced the tax base,[15] resulting in a plan to build the project in phases.

[18] In January 2012, SMART completed final negotiations to start rebuilding the 43-mile (69 km) Initial Operating Segment (IOS) between Airport Blvd Santa Rosa and the Civic Center Station in San Rafael at a cost less than originally budgeted.

[25][26][27] This resulted from lack of tax revenues due to the economic downturn, which also led to the project opening in phases.

[29] The agency additionally had been experiencing problems with warning systems at some grade crossings, and had not fully completed its approval process with the Federal Railroad Administration.

[28] The 2017 California floods caused damage to the Puerto Suello Hill Tunnel, further delaying testing of the line.

[33] In May 2013, the SMART board approved a resolution designating the San Rafael to Larkspur link as its "preferred alternative".

The agency submitted a letter to the Federal Transit Administration, and on September 24, 2013, SMART was accepted into its "Small Starts" program.

[40] Service gaps existed during the weekends of November 2019 between Petaluma to Novato–Hamilton as testing for the Downtown Novato station commenced.

[46][47] The agency planned to only resume 13 round trips on weekdays in an effort to lower costs with reduced ridership and an uncertain tax base.

[53] A letter to the city of Healdsburg in 2020 estimated the cost of reconstructing the Russian River bridge, building a new station, and rehabilitating the line at $32 million.

[58] On July 5, 2023, a grant was awarded by the California Transportation Commission, funded by the Road Repair and Accountability Act also known as SB1.

Not being member counties of the Sonoma–Marin Area Rail Transit District, a new funding mechanism would have to be established before service commenced.

[53] Also proposed is extending SMART north beyond Cloverdale to Ukiah[63] or the planned NWP terminus in Willits, where it would connect with the California Western Railroad and its tourist services.

[70] Freight operator NWP Co began to serve businesses along the SMART right-of-way between Lombard (at the Napa River) and Windsor in 2011.

"[72] In 2021, the agency was awarded a grant to help fund improvements in freight infrastructure, including new sidings and repairing the bridge over the Petaluma River.

However, SMART does not directly use these,[75] and all stops use newly constructed 48-inch (120 cm) high-floor platforms to allow level boarding onto and off of the train and provide accessibility.

[77][78] Stations typically include a small shelter with a peaked roof and a bench for seating; they also feature light poles, signs, and garbage cans.

The vehicles, designed specifically for SMART and another transit service, the Union Pearson Express in Toronto, Ontario, Canada, are slope-nosed and self-propelled by diesel engines that meet stringent "Tier 4" EPA requirements.

The agency did not accept the cars as delivered, and Nippon Sharyo dispatched a team to California to assess the damage and plan for repairs.

[89] In the original sales tax expenditure plan, $90 million was allocated for a bike/pedestrian path along the line for recreation and to enhance connections between stations and the developing network of bicycle-pedestrian pathways.

[90] As a result of the Great Recession of 2008, SMART changed its plans for the construction of the bicycle-pedestrian pathway as well as the rail project.

The Discounted fare is $0.75 plus $0.75 per zone[96] A monthly pass is also sold for $135 ($67.50 for eligible riders) which grants the bearer 31 days of unlimited travel from the date of first use.

[99] Until 2017, the Sonoma Raceway operated a race-day excursion service that used right-of-way owned by SMART, though not on the mainline tracks and using Amtrak equipment.

They concluded that Mansourian's demonstrated abilities during his temporary assignment coupled with his knowledge of California's permitting requirements and successful delivery of complex public works projects in Marin County made him the best candidate.