Microtubules (MTs) undergo various post-translational modifications, including polyglutamylation, which is the primary modification at unstructured C-terminal tubulin tails catalyzed by members of the tubulin tyrosine ligase-like (TTLL) protein family. In this report, we present the structural and functional characterization of TTLL11, the least studied member of the TTLL family. The cryoEM structure of the TTLL11/MT complex reveals a unique bipartite pattern of microtubule recognition, where the microtubule-binding and catalytic TTLL11 domains engage adjacent MT protofilaments. Biochemical experiments revealed a previously unknown glutamylation pattern, in which the polyglutamate tail directly extends the main chains of either α- or β-tubulin subunits. Finally, we have identified an intricate interplay between the enzymatic activities of TTLL11, TTL, and glutamate carboxypeptidases that governs selective modifications at individual tubulin protomers. Our work uncovers a novel type of tubulin polyglutamylation that expands the repertoire of known modifications comprising the 'tubulin code'. This code plays a major role in differentiating microtubules for distinct functions within cells and tissues.