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The project's cost and scope have long been a source of controversy. The project was presented to voters with a projected cost of $40 billion in 2008. Election year proponents also promised a 2028 completion date, and a $55 one-way Los Angeles to San Francisco fare. In 2012 the Authority re-estimated the project's year-of-expenditure cost at $68.4 billion. In 2012 the estimated cost of a fare from LA to San Francisco has risen to $86. In March 2018, the Authority revised its estimate to $77.3 billion and up to $98.1 billion, pushing initial service to 2029 and services from Los Angeles to San Francisco to 2033.

The Reason Foundation's Due Diligence Report (2008) projected that the final cost for the complete system (including both Phases I, II and an additional East Bay phase) would be $65.2 to $81.4 billion (2008). Current estimates from the Authority estimate a total cost for Phase 1 of $64.2 billion. The Authority is using Design-Build construction contracts to counter the tendency toward cost over-runs. All of the construction is to be done via "design-build" proposals wherein each builder is given leeway in the design and management of construction, but not the ability to run back with contract change orders except for extraordinary problems. The builder is given specifications but also given the freedom to meet them in their own way, plus the ability to modify the construction plans in an expeditious and cost-effective manner.

The California Legislative Analyst's Office published recommendations on May 10, 2011, which they said will help the high-speed rail project be developed successfully. They recommended that the California legislature seek flexibility on use of federal funds and then reconsider where construction of the high-speed rail line should start. They also recommended that the California legislature shift responsibility away from the Authority and fund only the administrative tasks of the Authority in the 2011–12 budget.

In January 2012, an independent peer review panel published a report recommending the Legislature not approve issuing $2.7 billion in bonds to fund the project. The panel of experts was created by state law to help safeguard the public's interest. The report said that moving ahead on the high-speed rail project without credible sources of adequate funding represents a financial risk to California.

Prior to the July 2012 vote, State Senator Joe Simitian, (D-Palo Alto), expressed concerns about financing needed to complete the project, asking: "Is there additional commitment of federal funds? There is not. Is there additional commitment of private funding? There is not. Is there a dedicated funding source that we can look to in the coming years? There is not." The lobbying and advocacy group Train Riders Association of California also considers that Bill SB 1029 "provides no high-speed service for the next decade".

In July 2014, The World Bank reported that the per kilometer cost of California's high-speed rail system was $56 million, more than double the average cost of $17–21 million per km of high speed rail in China and more than the $25–39 million per km average for similar projects in Europe. High real estate prices in California and three mountain ranges to cross contribute to the difference. For example, Construction Package 2-3 in the farmland of the flat Central Valley works out to $11.4 million per km, although this figure does not include electrification or property values, so it is roughly comparable internationally. Furthermore, the proposed High Speed 2 in Great Britain is estimated to be more expensive on a per mile basis than the Californian system.

As of May 2015, both construction packages awarded have come in significantly under staff estimates. For example, Construction Package 1 came in 20% under staff estimates ($985 million versus $1.2 billion), and Construction Package 2-3 came in under by 17% to 28% ($1.234567 billion versus $1.5–2 billion).

In December 2016, an internal-use-only draft risk assessment produced by the Federal Railroad Administration was delivered to the California Rail Authority which warned that the ICS (Merced-Bakersfield) segment could cost as much as $9.5 billion instead of the $6.4 billion originally budgeted, if certain challenges weren't addressed, including delays in environmental planning, lags in processing invoices and failures to acquire needed property. Federal Railroad Administration spokesman Matthew Lehner said that the draft risk assessment "is a standard oversight tool used on major capital projects — not just California", and he is confident the state can meet its deadline with continued focus and hard work. Concern over the article prompted the Authority to send a letter on January 13, 2017 to the Legislature that said that the characterization of cost overruns, delays, and potential lapses of funds are not borne out by the facts, and that other key federal findings were ignored. After downplaying risks of cost overruns, in January 2018 the Authority acknowledged that cost estimates for the initial segment had increased to $10.6 billion.