diff --git a/dev/tasks/r/github.linux.r-wasm.yml b/dev/tasks/r/github.linux.r-wasm.yml
new file mode 100644
index 000000000000..ee38740bb47d
--- /dev/null
+++ b/dev/tasks/r/github.linux.r-wasm.yml
@@ -0,0 +1,75 @@
+# Licensed to the Apache Software Foundation (ASF) under one
+# or more contributor license agreements.  See the NOTICE file
+# distributed with this work for additional information
+# regarding copyright ownership.  The ASF licenses this file
+# to you under the Apache License, Version 2.0 (the
+# "License"); you may not use this file except in compliance
+# with the License.  You may obtain a copy of the License at
+#
+#   http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing,
+# software distributed under the License is distributed on an
+# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
+# KIND, either express or implied.  See the License for the
+# specific language governing permissions and limitations
+# under the License.
+
+{% import 'macros.jinja' as macros with context %}
+
+{{ macros.github_header() }}
+
+jobs:
+  r-universe-wasm:
+    name: "R-universe Wasm build"
+    runs-on: ubuntu-latest
+    timeout-minutes: 60
+
+    steps:
+      {{ macros.github_checkout_arrow()|indent }}
+
+      - uses: r-lib/actions/setup-r@v2
+        with:
+          install-r: true
+
+      - name: Build Arrow R source package
+        shell: bash
+        run: |
+          cd arrow/r
+          make sync-cpp
+          R CMD build --no-build-vignettes .
+
+      - name: Pull the R-universe Wasm image
+        shell: bash
+        run: docker pull ghcr.io/r-universe-org/build-wasm:latest
+
+      - name: Build Wasm binary in the R-universe container
+        shell: bash
+        run: |
+          docker run --rm \
+            -v "${PWD}/arrow/r:/work" \
+            -w /work \
+            ghcr.io/r-universe-org/build-wasm:latest \
+            bash -lc '
+              set -euxo pipefail
+              R -q -e "if (!requireNamespace(\"pak\", quietly = TRUE)) install.packages(\"pak\", repos = \"https://cloud.r-project.org\"); if (!requireNamespace(\"rwasm\", quietly = TRUE)) pak::pak(\"r-wasm/rwasm\"); rwasm::build(\".\")" \
+                2>&1 | tee build-wasm.log
+            '
+
+      - name: List generated artifacts
+        if: always()
+        shell: bash
+        run: |
+          ls -lh arrow/r/arrow_*.tar.gz
+          ls -lh arrow/r/arrow_*.tgz || true
+          ls -lh arrow/r/build-wasm.log || true
+
+      - name: Upload Wasm build artifacts
+        if: always()
+        uses: actions/upload-artifact@v4
+        with:
+          name: r-wasm-build
+          path: |
+            arrow/r/arrow_*.tar.gz
+            arrow/r/arrow_*.tgz
+            arrow/r/build-wasm.log
diff --git a/dev/tasks/tasks.yml b/dev/tasks/tasks.yml
index 9647e5531da3..2d2b9ae39e41 100644
--- a/dev/tasks/tasks.yml
+++ b/dev/tasks/tasks.yml
@@ -651,6 +651,10 @@ tasks:
       env:
         CMAKE_BUILD_TYPE: MinSizeRel
 
+  test-r-wasm:
+    ci: github
+    template: r/github.linux.r-wasm.yml
+
   test-r-devdocs:
     ci: github
     template: r/github.devdocs.yml
diff --git a/r/inst/build_arrow_static.sh b/r/inst/build_arrow_static.sh
index 241994223d3e..349531b75fd9 100755
--- a/r/inst/build_arrow_static.sh
+++ b/r/inst/build_arrow_static.sh
@@ -62,9 +62,12 @@ case "$CXX" in
     ;;
 esac
 
+# Used for Emscripten
+: ${CMAKE_WRAPPER:=""}
+
 mkdir -p "${BUILD_DIR}"
 pushd "${BUILD_DIR}"
-${CMAKE} -DARROW_BOOST_USE_SHARED=OFF \
+${CMAKE_WRAPPER} ${CMAKE} -DARROW_BOOST_USE_SHARED=OFF \
     -DARROW_SNAPPY_USE_SHARED=OFF \
     -DARROW_BUILD_TESTS=OFF \
     -DARROW_BUILD_SHARED=OFF \
@@ -74,6 +77,8 @@ ${CMAKE} -DARROW_BOOST_USE_SHARED=OFF \
     -DARROW_CSV=ON \
     -DARROW_DATASET=${ARROW_DATASET:-ON} \
     -DARROW_DEPENDENCY_SOURCE=${ARROW_DEPENDENCY_SOURCE:-AUTO} \
+    -DARROW_DEPENDENCY_USE_SHARED=${ARROW_DEPENDENCY_USE_SHARED:-ON} \
+    -DARROW_ENABLE_THREADING=${ARROW_ENABLE_THREADING:-ON} \
     -DAWSSDK_SOURCE=${AWSSDK_SOURCE:-} \
     -DBoost_SOURCE=${Boost_SOURCE:-} \
     -Dlz4_SOURCE=${lz4_SOURCE:-} \
diff --git a/r/tools/nixlibs.R b/r/tools/nixlibs.R
index 947bb6c3f5cc..ba705e03ad7e 100644
--- a/r/tools/nixlibs.R
+++ b/r/tools/nixlibs.R
@@ -616,6 +616,7 @@ build_libarrow <- function(src_dir, dst_dir) {
   }
 
   env_var_list <- with_cloud_support(env_var_list)
+  env_var_list <- with_wasm_support(env_var_list)
 
   # turn_off_all_optional_features() needs to happen after
   # with_cloud_support(), since it might turn features ON.
@@ -883,6 +884,40 @@ is_feature_requested <- function(env_varname, env_var_list, default = env_is("LI
   requested
 }
 
+with_wasm_support <- function(env_var_list) {
+  cc <- env_var_list[["CC"]]
+  cxx <- env_var_list[["CXX"]]
+  if (!grepl("emcc", cc) && !grepl("em\\+\\+", cxx)) {
+    return(env_var_list)
+  }
+
+  lg("Emscripten compiler detected; configuring for WASM build", .indent = "****")
+
+  if (!nzchar(Sys.which("emcmake"))) {
+    stop("emcmake is required for Emscripten/webR builds but was not found in PATH")
+  }
+
+  wasm_overrides <- c(
+    CMAKE_WRAPPER = "emcmake",
+    ARROW_DEPENDENCY_SOURCE = "BUNDLED",
+    ARROW_DEPENDENCY_USE_SHARED = "OFF",
+    ARROW_ENABLE_THREADING = "OFF",
+    ARROW_GCS = "OFF",
+    ARROW_JEMALLOC = "OFF",
+    ARROW_MIMALLOC = "OFF",
+    ARROW_S3 = "OFF",
+    ARROW_WITH_BROTLI = "OFF",
+    ARROW_WITH_BZ2 = "OFF",
+    ARROW_WITH_ZSTD = "OFF",
+    N_JOBS = "2",
+    EXTRA_CMAKE_FLAGS = paste(
+      env_var_list[["EXTRA_CMAKE_FLAGS"]],
+      "-DARROW_SIMD_LEVEL=NONE -DARROW_RUNTIME_SIMD_LEVEL=NONE"
+    )
+  )
+  replace(env_var_list, names(wasm_overrides), wasm_overrides)
+}
+
 with_cloud_support <- function(env_var_list) {
   arrow_s3 <- is_feature_requested("ARROW_S3", env_var_list)
   arrow_gcs <- is_feature_requested("ARROW_GCS", env_var_list)