The train operator, which was taken over by the Scottish Government on Friday, only displays the price of single tickets for one-way journeys, even when buying a return would be cheaper.
This is despite Britain’s official National Rail Enquiries (NRE) website showing passengers return fares if they are cheaper than singles for one-way trips.
Ironically, the website then provides a link for customers to book the cheaper ticket via ScotRail’s website.
The Scottish Government’s Transport Scotland said ScotRail should do more to ensure passengers got the best fare.
After Scotland on Sunday raised the issue, ScotRail said its website operator was now “working on a fix”.
The ScotRail anomaly includes journeys between several stations in Glasgow – Britain’s biggest urban rail network outside London.
These include an off-peak one-way trip between Hyndland in the West End and Queen Street, for which a single ticket costs £2.70 but an off-peak return is only £2.40.
At Shettleston in the East End, a single to Queen Street is £3 while an off-peak return is £2.70.
On the south side, Mount Florida to Glasgow Central is £2.60 single but £2.40 off-peak return.
The anomaly is understood to be because such returns were heavily discounted historically to encourage off-peak travel.
There are even cheaper return tickets available on some routes for travel between 11am and 3pm on weekdays, but these are not shown on either the ScotRail or NRE websites when booking one-way journeys – the Hyndland-Queen Street one costs just £1.80.
Other such super off-peak day return tickets include £10.40 between Edinburgh and Glasgow compared to the off-peak single fare of £14.
One passenger said: "The issue at stake is passengers purchasing single tickets for some off-peak journeys are being charged more by the ScotRail website than if they purchase the same journey from ScotRail via the NRES website, which will assign them an off-peak return ticket when it is cheaper than the single fare.”
Passenger watchdog Transport Focus said: “We have asked ScotRail to investigate why this has occurred and are seeking assurances this issue is fixed.”
Senior stakeholder manager Robert Samson said: “It’s important passengers have confidence they can find the best deal when buying their ticket.
"Finding out you could have saved money if only you’d known where to look damages trust between passengers and train companies.”
Fares campaigner George Eckton, who has a lodged a Holyrood petition for passengers “to be given information on the cheapest possible fare as a matter of course”, said: “It’s the right thing to do for a service now directly delivered by ministers to tell the public the cheapest fare available."
A Transport Scotland spokesperson said: “We want more people to choose to travel by train on our publicly-controlled and operated railway, so need to feel confident they can book a ticket easily and they have got the best fare.
“ScotRail Trains Limited will be expected to explore what more can be done to achieve this.”
ScotRail commercial director Lesley Kane said: “We want our customers to travel quickly, easily and with the best-value ticket possible.
“We’re committed to ensuring rail fares are affordable and customers have easy access to best-value fares.”