After 1945, ridership declined with the rise in automobile use; in 1977 SP petitioned the state Public Utilities Commission to discontinue the commuter operation because of ongoing losses.

California legislators wrote Assembly Bill 1853 in 1977 to allow local transit districts along the line to make bulk purchases of tickets for resale at a loss, subsidizing commuters reliant on the Peninsula Commute until 1980; more importantly, the bill also authorized the California Department of Transportation (Caltrans) to begin negotiating with SP to operate the passenger rail service and acquire the right-of-way between San Bruno and Daly City.

Subsequently, San Mateo and Santa Clara Counties commissioned Earth Metrics, Inc., to prepare an Environmental Impact Report on right-of-way acquisition and expansion of operations.

Five months later, CalTrain increased the bicycle limit to 24 per train, making the service attractive to commuters in bicycle-friendly cities such as San Francisco and Palo Alto.

[11] In June 2003, a passenger connection for the Bay Area Rapid Transit (BART) and Caltrain systems opened at Millbrae station just south of the San Francisco International Airport.

Caltrain announced on August 19, 2011, a staff recommendation to sign a five-year, $62.5 million contract with TransitAmerica Services, after taking proposals from three other firms, including Amtrak California, which had provided operating employees since 1992.

[19][20] On February 17, 2017, California State Senator Jerry Hill introduced SB 797, which would permit the Peninsula Corridor Joint Powers Board to submit a regional measure for sales tax increase of 1⁄8th of one cent to the voters in the three counties served by Caltrain.

[21] The regional measure would require a two-thirds majority (aggregated among the three counties) to pass, and would provide Caltrain with a dedicated revenue source estimated at $100 million per year.

[28] The poll was sponsored by the Silicon Valley Leadership Group (SVLG), headed by Guardino, which predicted that daily ridership could rise to 250,000 with the improvements in service funded by the dedicated sales tax increase.

[28] By early 2020, the joint powers board was planning to propose a one-eighth-cent sales tax for voter approval later in the year, to provide an estimated $108 million of dedicated funding for the system, which currently relies on rider fares for 70% of its revenue.

[33] In July, after the San Francisco Board of Supervisors initially declined to consider the ballot proposal, citing concerns about the system's governance structure, Caltrain officials warned that the agency would run out of operating funds and be forced to suspend service by the end of the year.

[34][35][36] In August, San Mateo County officials agreed to make Caltrain more independent from SamTrans in exchange for placing the sales tax on the ballot.

[38] The schedule was adjusted again starting December 14, with slightly fewer weekday trains (68) but more frequent off-peak and weekend service to support essential workers.

Originally scheduled for completion by 2020,[43][45] the first electric multiple unit services started on August 11, 2024,[46] with full electrification achieved and diesel trains retired on September 21, 2024.

[58] On April 30, legislators in the United States Congress included $100 million for the Caltrain electrification project in the proposed 2017 federal spending bill, which was signed into law by President Trump on May 6.

[73]: 10  Grade separation projects near the Belmont and San Carlos stations (for Ralston, Harbor, Holly, Brittan, and Howard) were completed in 1995, and 2000;[73]: 10  these were "hybrid" crossings, executed as a combination of road depression and rails elevated on berms.

An alternative proposal, by then-Mayor Ed Lee, would see the existing terminal and trains yards demolished, along with Interstate 280 in Mission Bay, and replaced with infill housing.

A draft environmental impact report stated the lack of public transportation between Monterey County and the Bay Area has resulted in increased private commuter vehicle traffic.

[100] This project depends on state and federal funding availability, a possible local sales tax measure, and an agreement with Union Pacific, the owner of the Salinas-to-Gilroy tracks and right-of-way.

[101] This would complement another plan to re-establish rail service last provided by Southern Pacific's Del Monte Express which operated between Monterey and San Francisco.

[102] The switch to Capitol Corridor was cited as an advantage, since CCJPA had experience with commuter trains sharing service on Union Pacific-owned freight right-of-way.

[115] The Caltrain right of way between San Francisco and Tamien stations is owned and maintained by its operating agency, the Peninsula Corridor Joint Powers Board (PCJPB).

If passengers who use the Clipper card fail to tag off when they exit the train, they will be charged "the highest cash fare from [their] point of origin", including pass holders.

[176] Rather than writing the citation on the spot, which takes up to fifteen minutes, the conductor will scan the photo ID, and an administrative penalty will be mailed to the address on record, bypassing the civil superior court system.

[220] After September 2024, electric multiple units displaced the legacy diesel locomotive and passenger car fleet for service between San Francisco and Tamien.

[226][227] Caltrain has direct connections to three regional rail services; Bay Area Rapid Transit (BART) (with service to San Francisco, SFO, Oakland, Fremont, Richmond, Dublin, Concord, and Pittsburg) at Millbrae, Amtrak's Capitol Corridor and Coast Starlight trains, as well as the Altamont Corridor Express at San Jose Diridon station and the Santa Clara Transit Center.

(Additionally, Golden Gate Transit of Marin and Sonoma Counties is within 20 minutes' walking distance, or a short Muni ride via the N or T lines, from Caltrain's northern terminus.)

In addition to many bus connections, VTA light rail service has two other Caltrain transfer points at San Jose's Tamien and at Mountain View.

Muni intended to establish another light rail connection to the Bayshore station at Visitacion Valley in southern San Francisco for the T Third line, but this has been delayed indefinitely due to cost and design issues.

[citation needed] If the aforementioned Downtown Rail Extension (now known as The Portal) is completed, the underground walkway between the Salesforce Transit Center and Embarcadero station would also connect Caltrain to Muni Metro's F Market & Wharves, J Church, K Ingleside, and M Ocean View, as well as providing a second connection to the N Judah and linking Caltrain with the California street cable car line.