Dyer’s side – hit by two covid cases in the build-up to the match – threw away a 2-0 lead at Rugby Park for their third consecutive loss and eighth in the last 11 matches.
Killie occupy ninth place in the Scottish Premiership table - five points from the bottom – but a lack of wins had piled pressure onto the manager with just four recorded in the league since the start of October.
Dyer had sounded increasingly resigned and frustrated in recent weeks, and both he and the Rugby Park bosses reached the same conclusion in the wake of the latest efeat.
The club confirmed the Englishman’s departure in a statement: “Kilmarnock Football Club can confirm the departure of manager Alex Dyer by mutual consent following today’s 3-2 defeat to St Johnstone.
“We are grateful to Alex for all he has achieved with the club since joining Killie in October 2017. However, recent results and performances have been disappointing and with 24 points from 25 Premiership matches, we believe this is the right time for a change.
“Alex was part of the management team which secured back-to-back club record points totals in 2017/18 and 2018/19 and a return to European football at Rugby Park.
“The club will make no further comment at this time while the Board are fully focused on securing a replacement."
Dyer was brought to Scottish football by Steve Clarke during his tenure as Killie manager. He continued as assistant to Angelo Alessio and assumed the reins when the Italian was dismissed just over a year ago.
Chairman Billy Bowie said: “This was a tough decision for the club and not one which was made lightly. However in light of recent results and in the interest of preserving our Scottish Premiership status, we feel this is the correct time for a change.
“Alex is a great man who I have the utmost respect for and he will always be warmly welcomed back to Rugby Park.
“I want to thank Alex for his important contribution to some truly wonderful days here at Kilmarnock and I wish him every success in the future.”