Many prokaryotes use swimming motility to move toward favorable conditions and escape adverse surroundings. Regulatory mechanisms governing bacterial flagella-driven motility are well-established, however, little is yet known about the regulation underlying swimming motility propelled by the archaeal cell surface structure, the archaella. Previous research showed that deletion of the adhesion pilins (PilA1-6), subunits of the type IV pili cell surface structure, renders the model archaeon non-motile. In this study, we used EMS mutagenesis and a motility assay to identify motile suppressors of the Δ[] strain. Of the eight suppressors identified, six contain missense mutations in archaella biosynthesis genes, and . Overexpression of these and mutant constructs in the respective multi-deletion strains Δ[]Δ and Δ[]Δ confirmed their role in suppressing the Δ[] motility defect. Additionally, three suppressors harbor co-occurring disruptive missense and nonsense mutations in , a gene encoding a proposed regulatory protein. A deletion of resulted in hypermotility, while overexpression in wild-type cells led to decreased motility. Moreover, qRT-PCR analysis revealed that in wild-type cells, higher expression levels of , , and the archaellin gene were observed in motile early-log phase rod-shaped cells compared to non-motile mid-log phase disk-shaped cells. Conversely, Δ cells, which form rods during both early and mid-log phases, exhibited similar expression levels of genes in both growth phases. Our findings contribute to a deeper understanding of the mechanisms governing archaeal motility, highlighting the involvement of ArlI, ArlJ, and CirA in pilin-mediated motility regulation.