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Creating artificial cells with a dynamic cytoskeleton, akin to those in living cells, is a major goal in bottom‐up synthetic biology. In this study, we demonstrate the in situ polymerization of microtubules encapsulated in giant polymer‐lipid hybrid vesicles (GHVs) composed of 1,2‐dioleoyl‐sn‐glycero‐3‐phosphocholine and an amphiphilic block copolymer. The block copolymer is comprised of poly(cholesteryl methacrylate‐co‐butyl methacrylate) as the hydrophobic block and either poly(6‐O‐methacryloyl‐D‐galactopyranose) or poly(carboxyethyl acrylate) as the hydrophilic extension. Depending on the concentrations of guanosine triphosphate (GTP) or its slowly hydrolyzable analog, guanosine‐5′‐[(α,β)‐methyleno]triphosphate (GMPCPP), different microtubule morphologies are observed, including encapsulated microtubule networks, spike protrusions, as well as membrane‐associated or aggregated microtubules. Overall, this work represents a step forward in mimicking the cellular cytoskeletons and uncovering the influence of membrane composition on microtubule morphologies.