It was founded in 1980 as a county-run oversight and funding agency for a group of private contract operators which had previously provided such services on their own.

In Central Suffolk, the East Patchogue-based Louis A. Fuoco Bus Line (1962-1992) served Patchogue, East Patchogue, Hagerman, Bellport, South Haven, Mastic, Mastic Beach, Port Jefferson, Medford, Coram, Ridge, Calverton, and Riverhead.

Quinn's Bus Lines, and later Coram Bus Service after the two were merged in 1969,[5] mainly served the area between Port Jefferson and Wading River; especially after the demise of the Wading River Extension of the Port Jefferson Branch.

[7] On the east end, Sunrise Coach Lines (1946–present), which served Greenport, Riverhead, Southampton, Sag Harbor, and Easthampton, began operations in 1946, continued in existence under contract with joint venture Twin Forks Transit for the routes they originally operated for Suffolk County Transit.

[8] As of 10/29/23, the Twin Forks Joint Venture has been discontinued as it is no longer needed due to the discontinuation of the S92, which was co-operated by Sunrise and Hampton Jitney Utility Lines, a Bee Line Incorporated subsidiary, ran from Patchogue along Montauk Highway into Merrick Road in Nassau County.

Alert Coach, an affiliate of Baumann & Sons Buses, Incorporated, and Acme Bus Corporation began on November 30, 1966, and had at least four lines within the county, which included a troubled history with the Suffolk portion of the old Utility Lines bus.

The fare hike took place on June 17, 2011, with Sunday service operating from July until September.

Because of this, NICE bus made a change to weekend service on the n71 bus route in September 2023 (and now daily as of summer 2024) to provide a connection to the timed transfer point at Amityville from the Sunrise Mall in Nassau County, where both the n71 and S20 (now route 2) previously terminated.

The current Suffolk County Transit base fare for most one-way local bus travel is $2.25.

Undergraduate students of Stony Brook University (which prepays for the rides at the start of the school year so that it does not have to run its own buses) may ride to Smith Haven Mall on Route 51 for free, with a valid SBU ID, on weekends.

Fare payment is conducted with Suffolk Transit bus tokens, coins or paper currency, or via the FastFare app.

When both are running, route 77 (regular daily service), combined with the 77Y (weekday peak hours) operate alternately every 30 minutes between Patchogue and Sunshine Square.

Effective October 29, 2023, the Suffolk County Transit Redesign removed the "S" prefix from all routes.