diff --git a/changelog.d/9610.docker b/changelog.d/9610.docker
new file mode 100644
index 000000000000..056252a66963
--- /dev/null
+++ b/changelog.d/9610.docker
@@ -0,0 +1 @@
+Speed up Docker builds and make it nicer to test against Complement while developing (install all dependencies before copying the project).
diff --git a/docker/Dockerfile b/docker/Dockerfile
index def4501541fe..3b3bf403d54b 100644
--- a/docker/Dockerfile
+++ b/docker/Dockerfile
@@ -30,31 +30,29 @@ RUN apt-get update && apt-get install -y \
     libxslt1-dev \
     rustc \
     zlib1g-dev \
- && rm -rf /var/lib/apt/lists/*
+    && rm -rf /var/lib/apt/lists/*
 
-# Build dependencies that are not available as wheels, to speed up rebuilds
-RUN pip install --prefix="/install" --no-warn-script-location \
-        cryptography \
-        frozendict \
-        jaeger-client \
-        opentracing \
-        # Match the version constraints of Synapse
-        "prometheus_client>=0.4.0" \
-        psycopg2 \
-        pycparser \
-        pyrsistent \
-        pyyaml \
-        simplejson \
-        threadloop \
-        thrift
-
-# now install synapse and all of the python deps to /install.
-COPY synapse /synapse/synapse/
+# Copy just what we need to pip install
 COPY scripts /synapse/scripts/
 COPY MANIFEST.in README.rst setup.py synctl /synapse/
+COPY synapse/__init__.py /synapse/synapse/__init__.py
+COPY synapse/python_dependencies.py /synapse/synapse/python_dependencies.py
 
+# To speed up rebuilds, install all of the dependencies before we copy over
+# the whole synapse project so that we this layer in the Docker cache can be
+# used while you develop on the source
+#
+# This is aiming at installing the `install_requires` and `extras_require` from `setup.py`
 RUN pip install --prefix="/install" --no-warn-script-location \
-        /synapse[all]
+    /synapse[all]
+
+# Copy over the rest of the project
+COPY synapse /synapse/synapse/
+
+# Install the synapse package itself and all of its children packages.
+#
+# This is aiming at installing only the `packages=find_packages(...)` from `setup.py
+RUN pip install --prefix="/install" --no-deps --no-warn-script-location /synapse
 
 ###
 ### Stage 1: runtime
@@ -70,7 +68,7 @@ RUN apt-get update && apt-get install -y \
     libwebp6 \
     xmlsec1 \
     libjemalloc2 \
- && rm -rf /var/lib/apt/lists/*
+    && rm -rf /var/lib/apt/lists/*
 
 COPY --from=builder /install /usr/local
 COPY ./docker/start.py /start.py
@@ -83,4 +81,4 @@ EXPOSE 8008/tcp 8009/tcp 8448/tcp
 ENTRYPOINT ["/start.py"]
 
 HEALTHCHECK --interval=1m --timeout=5s \
-  CMD curl -fSs http://localhost:8008/health || exit 1
+    CMD curl -fSs http://localhost:8008/health || exit 1