[9] In February 2020, Gilruth joined the Scottish Government as Minister for Europe, Migration and International Development as part of the reshuffle following the resignation of Cabinet Secretary for Finance Derek Mackay.

[11][12] She said: "The transport portfolio is an exciting opportunity to not just shape the infrastructure of our country but to also help Scotland become a world leader in achieving our goal to become net zero by 2045.

[14][15] Following Yousaf's resignation as First Minister and Leader of the Scottish National Party in May 2024, Gilruth retained the post of Cabinet Secretary for Education in the Swinney government.

[16] Gilruth came under criticism in February 2024 as it became to light that she had not read a report into violence in schools in the Aberdeen City Council area.

[17] Addressing the comments made by an EIS spokesperson, Gilruth said that the report would "be for Aberdeen City Council to respond to", and also highlighted her awareness around the "challenges on this matter".

[18] In September 2024, she stated that the quality of debate in the Scottish Parliament could be improved by limiting the use of mobile phones and tablets among MSPs.