Annuals 10–40 cm. Stems erect to ascending. Leaf blades linear to narrowly oblanceolate, length usually 6+ times width, margins entire, subentire, or ± dentate. Inflorescences finely scaly and spreading-glandular; nodes 1–3(–5)-flowered; flowers not crowded; distalmost bracts linear, 2–5 mm. Pedicels ascending, longer than calyx, visible. Flowers: caly× lobes lanceolate to ovate, equal to capsule, ape× subacute to slightly rounded; corolla white to blue-purple, 8–12(–15) mm, length 2+ times calyx, glandular; banner length 0.8–1 times wings, base with folds bulging 0.5 mm away from throat opening, reflexed portion length 1.5–2 times throat; throat strongly angled to tube, as wide as long, pouch ± square, prominent; stamens: abaxial filaments glabrous, adaxials hairy at base, basal spur 0(or 1). Seeds 2–4(–6), round to oblong, 1.5–2.2 mm, margins thin, scarcely inrolled. 2n = 14.
Phenology: Flowering (Apr–)May–Jul.
Habitat: Open coniferous forests.
Elevation: 200–2000 m.
Collinsia linearis and C. rattanii occupy similar habitats, often growing in rocky soil derived from mafic, volcanic rock. They form a lineage but may not be reciprocally monophyletic (B. G. Baldwin et al. 2011). Other than differences in corolla size and shape, and, possibly, seed morphology, they are extremely similar. Corolla shape (floor of throat angled 45° to 60° from abaxial side of caly× and reflexed portion of adaxial lip length 1.5 to 2 times throat) and smaller corolla size are characteristic of C. linearis. Some plants from this lineage, mostly from Oregon, are difficult to assign to either C. linearis or C. rattanii.
Specimens annotated as Collinsia linearis from British Columbia have not been verified.