diff --git a/.github/workflows/continous-delivery.yml b/.github/workflows/continous-delivery.yml
index 1adb5297d70..97a10ebf40d 100644
--- a/.github/workflows/continous-delivery.yml
+++ b/.github/workflows/continous-delivery.yml
@@ -77,6 +77,28 @@ jobs:
       zebra_skip_ipv6_tests: '1'
       rust_log: info
 
+  # Test that Zebra works using the default config with the latest Zebra version
+  test-configuration-file:
+    name: Test Zebra default Docker config file
+    timeout-minutes: 5
+    runs-on: ubuntu-latest
+    needs: build
+    steps:
+      - name: Inject slug/short variables
+        uses: rlespinasse/github-slug-action@v4
+        with:
+          short-length: 7
+
+      - name: Run tests using the default config
+        run: |
+          set -ex
+          docker pull ${{ env.GAR_BASE }}/zebrad@${{ needs.build.outputs.image_digest }}
+          docker run --detach --name default-conf-tests -t ${{ env.GAR_BASE }}/zebrad@${{ needs.build.outputs.image_digest }}
+          EXIT_STATUS=$(docker logs --tail all --follow default-conf-tests 2>&1 | grep -q --extended-regexp --max-count=1 -e 'estimated progress to chain tip.*BeforeOverwinter'; echo $?; )
+          docker stop default-conf-tests
+          docker logs default-conf-tests
+          exit "$EXIT_STATUS"
+
   # This jobs handles the deployment of a Managed Instance Group (MiG) with 2 nodes in
   # the us-central1 region. Two different groups of MiGs are deployed one for pushes to
   # the main branch and another for version releases of Zebra
@@ -90,7 +112,7 @@ jobs:
   # - on every release, when it's published
   deploy-nodes:
     name: Deploy ${{ inputs.network || 'Mainnet' }} nodes
-    needs: [ build, versioning ]
+    needs: [ build, test-configuration-file, versioning ]
     runs-on: ubuntu-latest
     timeout-minutes: 30
     permissions:
@@ -184,7 +206,7 @@ jobs:
   # Note: this instances are not automatically replaced or deleted
   deploy-instance:
     name: Deploy single instance
-    needs: build
+    needs: [ build, test-configuration-file ]
     runs-on: ubuntu-latest
     timeout-minutes: 30
     permissions:
diff --git a/.github/workflows/continous-integration-docker.patch.yml b/.github/workflows/continous-integration-docker.patch.yml
index c0a34842233..ae7f8f2a894 100644
--- a/.github/workflows/continous-integration-docker.patch.yml
+++ b/.github/workflows/continous-integration-docker.patch.yml
@@ -66,6 +66,18 @@ jobs:
     steps:
       - run: 'echo "No build required"'
 
+  test-configuration-file:
+    name: Test Zebra default Docker config file
+    runs-on: ubuntu-latest
+    steps:
+      - run: 'echo "No build required"'
+
+  test-zebra-conf-path:
+    name: Test Zebra custom Docker config file
+    runs-on: ubuntu-latest
+    steps:
+      - run: 'echo "No build required"'
+
   test-stateful-sync:
     name: Zebra checkpoint update / Run sync-past-checkpoint test
     runs-on: ubuntu-latest
diff --git a/.github/workflows/continous-integration-docker.yml b/.github/workflows/continous-integration-docker.yml
index 2b42f717be3..233302e4096 100644
--- a/.github/workflows/continous-integration-docker.yml
+++ b/.github/workflows/continous-integration-docker.yml
@@ -299,6 +299,54 @@ jobs:
         env:
           ZEBRA_TEST_LIGHTWALLETD: '1'
 
+  # Test that Zebra works using the default config with the latest Zebra version
+  test-configuration-file:
+    name: Test Zebra default Docker config file
+    timeout-minutes: 5
+    runs-on: ubuntu-latest
+    needs: build
+    if: ${{ github.event.inputs.regenerate-disks != 'true' && github.event.inputs.run-full-sync != 'true' && github.event.inputs.run-lwd-sync != 'true' && github.event.inputs.run-lwd-send-tx != 'true' }}
+    steps:
+      - name: Inject slug/short variables
+        uses: rlespinasse/github-slug-action@v4
+        with:
+          short-length: 7
+
+      - name: Run tests using the default config
+        run: |
+          set -ex
+          docker pull ${{ env.GAR_BASE }}/${{ env.IMAGE_NAME }}:sha-${{ env.GITHUB_SHA_SHORT }}
+          docker run --detach --name default-conf-tests -t ${{ env.GAR_BASE }}/${{ env.IMAGE_NAME }}:sha-${{ env.GITHUB_SHA_SHORT }} zebrad start
+          EXIT_STATUS=$(docker logs --tail all --follow default-conf-tests 2>&1 | grep -q --extended-regexp --max-count=1 -e 'estimated progress to chain tip.*BeforeOverwinter'; echo $?; )
+          docker stop default-conf-tests
+          docker logs default-conf-tests
+          exit "$EXIT_STATUS"
+
+  # Test that Zebra works using the $ZEBRA_CONF_PATH config
+  test-zebra-conf-path:
+    name: Test Zebra custom Docker config file
+    timeout-minutes: 5
+    runs-on: ubuntu-latest
+    needs: build
+    if: ${{ github.event.inputs.regenerate-disks != 'true' && github.event.inputs.run-full-sync != 'true' && github.event.inputs.run-lwd-sync != 'true' && github.event.inputs.run-lwd-send-tx != 'true' }}
+    steps:
+      - name: Inject slug/short variables
+        uses: rlespinasse/github-slug-action@v4
+        with:
+          short-length: 7
+
+      - name: Run tests using the $ZEBRA_CONF_PATH
+        run: |
+          set -ex
+          docker pull ${{ env.GAR_BASE }}/${{ env.IMAGE_NAME }}:sha-${{ env.GITHUB_SHA_SHORT }}
+          docker run --detach -e ZEBRA_CONF_PATH --name variable-conf-tests -t ${{ env.GAR_BASE }}/${{ env.IMAGE_NAME }}:sha-${{ env.GITHUB_SHA_SHORT }} -c $ZEBRA_CONF_PATH start
+          EXIT_STATUS=$(docker logs --tail all --follow variable-conf-tests 2>&1 | grep -q --extended-regexp --max-count=1 -e 'v1.0.0-rc.2.toml'; echo $?; )
+          docker stop variable-conf-tests
+          docker logs variable-conf-tests
+          exit "$EXIT_STATUS"
+        env:
+          ZEBRA_CONF_PATH: 'zebrad/tests/common/configs/v1.0.0-rc.2.toml'
+
   # zebrad cached checkpoint state tests
 
   # Regenerate mandatory checkpoint Zebra cached state disks.
diff --git a/docker/Dockerfile b/docker/Dockerfile
index c3689b1f0e9..c2c0c3d6e9c 100644
--- a/docker/Dockerfile
+++ b/docker/Dockerfile
@@ -104,13 +104,13 @@ RUN cargo chef cook --release --features sentry,lightwalletd-grpc-tests --worksp
 
 COPY . .
 RUN cargo test --locked --release --features lightwalletd-grpc-tests --workspace --no-run
+RUN cp /opt/zebrad/target/release/zebrad /usr/local/bin
 
 COPY ./docker/entrypoint.sh /
 RUN chmod u+x /entrypoint.sh
 
 # By default, runs the entrypoint tests specified by the environmental variables (if any are set)
 ENTRYPOINT [ "/entrypoint.sh" ]
-CMD [ "cargo" ]
 
 # In this stage we build a release (generate the zebrad binary)
 #
@@ -140,12 +140,15 @@ ARG CHECKPOINT_SYNC=true
 ARG NETWORK=Mainnet
 
 # Use a configurable dir and file for the zebrad configuration file
-ARG ZEBRA_CONF_PATH=/etc/zebra
-ENV ZEBRA_CONF_PATH ${ZEBRA_CONF_PATH}
+ARG ZEBRA_CONF_DIR=/etc/zebra
+ENV ZEBRA_CONF_DIR ${ZEBRA_CONF_DIR}
 
 ARG ZEBRA_CONF_FILE=zebrad.toml
 ENV ZEBRA_CONF_FILE ${ZEBRA_CONF_FILE}
 
+ARG ZEBRA_CONF_PATH=${ZEBRA_CONF_DIR}/${ZEBRA_CONF_FILE}
+ENV ZEBRA_CONF_PATH ${ZEBRA_CONF_PATH}
+
 # Build the `zebrad.toml` before starting the container, using the arguments from build
 # time, or using the default values set just above. And create the conf path and file if
 # it does not exist.
@@ -160,8 +163,8 @@ ENV ZEBRA_CONF_FILE ${ZEBRA_CONF_FILE}
 #  - move this file creation to an entrypoint as we can use default values at runtime,
 #    and modify those as needed when starting the container (at runtime and not at build time)
 #  - make `cache_dir`, `rpc.listen_addr`, `metrics.endpoint_addr`, and `tracing.endpoint_addr` into Docker arguments
-RUN mkdir -p ${ZEBRA_CONF_PATH} \
-    && touch ${ZEBRA_CONF_PATH}/${ZEBRA_CONF_FILE}
+RUN mkdir -p ${ZEBRA_CONF_DIR} \
+    && touch ${ZEBRA_CONF_PATH}
 RUN set -ex; \
   { \
     echo "[network]"; \
@@ -177,7 +180,7 @@ RUN set -ex; \
     echo "#endpoint_addr = '127.0.0.1:9999'"; \
     echo "[tracing]"; \
     echo "#endpoint_addr = '127.0.0.1:3000'"; \
-  } > "${ZEBRA_CONF_PATH}/${ZEBRA_CONF_FILE}"
+  } > "${ZEBRA_CONF_PATH}"
 
 EXPOSE 8233 18233
 
@@ -188,4 +191,4 @@ ARG SENTRY_DSN
 ENV SENTRY_DSN ${SENTRY_DSN}
 
 # TODO: remove the specified config file location and use the default expected by zebrad
-CMD zebrad -c "${ZEBRA_CONF_PATH}/${ZEBRA_CONF_FILE}" start
+CMD zebrad -c "${ZEBRA_CONF_PATH}" start
diff --git a/docker/entrypoint.sh b/docker/entrypoint.sh
index b7fa28f15c3..e17bfbcc163 100755
--- a/docker/entrypoint.sh
+++ b/docker/entrypoint.sh
@@ -15,7 +15,10 @@ echo "ZEBRA_CACHED_STATE_DIR=$ZEBRA_CACHED_STATE_DIR"
 echo "LIGHTWALLETD_DATA_DIR=$LIGHTWALLETD_DATA_DIR"
 
 case "$1" in
-    -- | cargo)
+    --* | -*)
+        exec zebrad "$@"
+        ;;
+    *)
         # For these tests, we activate the gRPC feature to avoid recompiling `zebrad`,
         # but we might not actually run any gRPC tests.
         if [[ "$RUN_ALL_TESTS" -eq "1" ]]; then
@@ -86,17 +89,7 @@ case "$1" in
             # Starting with a cached Zebra tip, test sending a block to Zebra's RPC port.
             ls -lh "$ZEBRA_CACHED_STATE_DIR"/*/* || (echo "No $ZEBRA_CACHED_STATE_DIR/*/*"; ls -lhR  "$ZEBRA_CACHED_STATE_DIR" | head -50 || echo "No $ZEBRA_CACHED_STATE_DIR directory")
             cargo test --locked --release --features getblocktemplate-rpcs --package zebrad --test acceptance -- --nocapture --include-ignored submit_block
-
-        # These command-lines are provided by the caller.
-        #
-        # TODO: test that the following 3 cases actually work, or remove them
         else
             exec "$@"
         fi
-        ;;
-    zebrad)
-        exec zebrad "$@"
-        ;;
-    *)
-        exec "$@"
 esac