diff --git a/cypress/e2e/register/email.spec.ts b/cypress/e2e/register/email.spec.ts
index a93c05c6ee..988cee9ff2 100644
--- a/cypress/e2e/register/email.spec.ts
+++ b/cypress/e2e/register/email.spec.ts
@@ -29,7 +29,7 @@ describe("Email Registration", () => {
             cy.startHomeserver({
                 template: "email",
                 variables: {
-                    SMTP_HOST: "host.docker.internal",
+                    SMTP_HOST: "{{HOST_DOCKER_INTERNAL}}", // This will get replaced in synapseStart
                     SMTP_PORT: _mailhog.instance.smtpPort,
                 },
             }).then((_homeserver) => {
diff --git a/cypress/plugins/docker/index.ts b/cypress/plugins/docker/index.ts
index 66bab0b853..4c2da5f645 100644
--- a/cypress/plugins/docker/index.ts
+++ b/cypress/plugins/docker/index.ts
@@ -156,6 +156,14 @@ export function isPodman(): Promise<boolean> {
     });
 }
 
+/**
+ * Supply the right hostname to use to talk to the host machine. On Docker this
+ * is "host.docker.internal" and on Podman this is "host.containers.internal".
+ */
+export async function hostContainerName() {
+    return (await isPodman()) ? "host.containers.internal" : "host.docker.internal";
+}
+
 /**
  * @type {Cypress.PluginConfig}
  */
diff --git a/cypress/plugins/synapsedocker/index.ts b/cypress/plugins/synapsedocker/index.ts
index a802c03939..7c278610cc 100644
--- a/cypress/plugins/synapsedocker/index.ts
+++ b/cypress/plugins/synapsedocker/index.ts
@@ -24,7 +24,7 @@ import * as fse from "fs-extra";
 import PluginEvents = Cypress.PluginEvents;
 import PluginConfigOptions = Cypress.PluginConfigOptions;
 import { getFreePort } from "../utils/port";
-import { dockerExec, dockerLogs, dockerRun, dockerStop } from "../docker";
+import { dockerExec, dockerLogs, dockerRun, dockerStop, hostContainerName, isPodman } from "../docker";
 import { HomeserverConfig, HomeserverInstance } from "../utils/homeserver";
 import { StartHomeserverOpts } from "../../support/homeserver";
 
@@ -58,27 +58,41 @@ async function cfgDirFromTemplate(opts: StartHomeserverOpts): Promise<Homeserver
     const baseUrl = `http://localhost:${port}`;
 
     // now copy homeserver.yaml, applying substitutions
-    console.log(`Gen ${path.join(templateDir, "homeserver.yaml")}`);
-    let hsYaml = await fse.readFile(path.join(templateDir, "homeserver.yaml"), "utf8");
+    const templateHomeserver = path.join(templateDir, "homeserver.yaml");
+    const outputHomeserver = path.join(tempDir, "homeserver.yaml");
+    console.log(`Gen ${templateHomeserver} -> ${outputHomeserver}`);
+    let hsYaml = await fse.readFile(templateHomeserver, "utf8");
     hsYaml = hsYaml.replace(/{{REGISTRATION_SECRET}}/g, registrationSecret);
     hsYaml = hsYaml.replace(/{{MACAROON_SECRET_KEY}}/g, macaroonSecret);
     hsYaml = hsYaml.replace(/{{FORM_SECRET}}/g, formSecret);
     hsYaml = hsYaml.replace(/{{PUBLIC_BASEURL}}/g, baseUrl);
     hsYaml = hsYaml.replace(/{{OAUTH_SERVER_PORT}}/g, opts.oAuthServerPort?.toString());
+    hsYaml = hsYaml.replace(/{{HOST_DOCKER_INTERNAL}}/g, await hostContainerName());
     if (opts.variables) {
+        let fetchedHostContainer = null;
         for (const key in opts.variables) {
-            hsYaml = hsYaml.replace(new RegExp("%" + key + "%", "g"), String(opts.variables[key]));
+            let value = String(opts.variables[key]);
+
+            if (value === "{{HOST_DOCKER_INTERNAL}}") {
+                if (!fetchedHostContainer) {
+                    fetchedHostContainer = await hostContainerName();
+                }
+                value = fetchedHostContainer;
+            }
+
+            hsYaml = hsYaml.replace(new RegExp("%" + key + "%", "g"), value);
         }
     }
 
-    await fse.writeFile(path.join(tempDir, "homeserver.yaml"), hsYaml);
+    await fse.writeFile(outputHomeserver, hsYaml);
 
     // now generate a signing key (we could use synapse's config generation for
     // this, or we could just do this...)
     // NB. This assumes the homeserver.yaml specifies the key in this location
     const signingKey = randB64Bytes(32);
-    console.log(`Gen ${path.join(templateDir, "localhost.signing.key")}`);
-    await fse.writeFile(path.join(tempDir, "localhost.signing.key"), `ed25519 x ${signingKey}`);
+    const outputSigningKey = path.join(tempDir, "localhost.signing.key");
+    console.log(`Gen -> ${outputSigningKey}`);
+    await fse.writeFile(outputSigningKey, `ed25519 x ${signingKey}`);
 
     return {
         port,
@@ -88,27 +102,38 @@ async function cfgDirFromTemplate(opts: StartHomeserverOpts): Promise<Homeserver
     };
 }
 
-// Start a synapse instance: the template must be the name of
-// one of the templates in the cypress/plugins/synapsedocker/templates
-// directory
+/**
+ * Start a synapse instance: the template must be the name of
+ * one of the templates in the cypress/plugins/synapsedocker/templates
+ * directory.
+ *
+ * Any value in opts.variables that is set to `{{HOST_DOCKER_INTERNAL}}'
+ * will be replaced with 'host.docker.internal' (if we are on Docker) or
+ * 'host.containers.interal' if we are on Podman.
+ */
 async function synapseStart(opts: StartHomeserverOpts): Promise<HomeserverInstance> {
     const synCfg = await cfgDirFromTemplate(opts);
 
     console.log(`Starting synapse with config dir ${synCfg.configDir}...`);
 
+    const dockerSynapseParams = ["--rm", "-v", `${synCfg.configDir}:/data`, "-p", `${synCfg.port}:8008/tcp`];
+
+    if (await isPodman()) {
+        // Make host.containers.internal work to allow Synapse to talk to the
+        // test OIDC server.
+        dockerSynapseParams.push("--network");
+        dockerSynapseParams.push("slirp4netns:allow_host_loopback=true");
+    } else {
+        // Make host.docker.internal work to allow Synapse to talk to the test
+        // OIDC server.
+        dockerSynapseParams.push("--add-host");
+        dockerSynapseParams.push("host.docker.internal:host-gateway");
+    }
+
     const synapseId = await dockerRun({
         image: "matrixdotorg/synapse:develop",
         containerName: `react-sdk-cypress-synapse`,
-        params: [
-            "--rm",
-            "-v",
-            `${synCfg.configDir}:/data`,
-            "-p",
-            `${synCfg.port}:8008/tcp`,
-            // make host.docker.internal work to allow Synapse to talk to the test OIDC server
-            "--add-host",
-            "host.docker.internal:host-gateway",
-        ],
+        params: dockerSynapseParams,
         cmd: ["run"],
     });
 
diff --git a/cypress/plugins/synapsedocker/templates/default/homeserver.yaml b/cypress/plugins/synapsedocker/templates/default/homeserver.yaml
index a866d4b5be..e51ac1918f 100644
--- a/cypress/plugins/synapsedocker/templates/default/homeserver.yaml
+++ b/cypress/plugins/synapsedocker/templates/default/homeserver.yaml
@@ -81,9 +81,10 @@ oidc_providers:
       issuer: "http://localhost:{{OAUTH_SERVER_PORT}}/oauth"
       authorization_endpoint: "http://localhost:{{OAUTH_SERVER_PORT}}/oauth/auth.html"
       # the token endpoint receives requests from synapse, rather than the webapp, so needs to escape the docker container.
-      # Hence, host.docker.internal rather than localhost.
-      token_endpoint: "http://host.docker.internal:{{OAUTH_SERVER_PORT}}/oauth/token"
-      userinfo_endpoint: "http://host.docker.internal:{{OAUTH_SERVER_PORT}}/oauth/userinfo"
+      # Hence, HOST_DOCKER_INTERNAL rather than localhost. This is set to
+      # host.docker.internal on Docker and host.containers.internal on Podman.
+      token_endpoint: "http://{{HOST_DOCKER_INTERNAL}}:{{OAUTH_SERVER_PORT}}/oauth/token"
+      userinfo_endpoint: "http://{{HOST_DOCKER_INTERNAL}}:{{OAUTH_SERVER_PORT}}/oauth/userinfo"
       client_id: "synapse"
       discover: false
       scopes: ["profile"]
diff --git a/cypress/support/homeserver.ts b/cypress/support/homeserver.ts
index 9f5e46efb0..2e8a309a65 100644
--- a/cypress/support/homeserver.ts
+++ b/cypress/support/homeserver.ts
@@ -39,15 +39,22 @@ declare global {
         interface Chainable {
             /**
              * Start a homeserver instance with a given config template.
+             *
              * @param opts: either the template path (within cypress/plugins/{homeserver}docker/template/), or
              *   an options object
+             *
+             * If any of opts.variables has the special value
+             * '{{HOST_DOCKER_INTERNAL}}', it will be replaced by
+             * 'host.docker.interal' if we are on Docker, or
+             * 'host.containers.internal' on Podman.
              */
             startHomeserver(opts: string | StartHomeserverOpts): Chainable<HomeserverInstance>;
 
             /**
              * Custom command wrapping task:{homeserver}Stop whilst preventing uncaught exceptions
              * for if Homeserver stopping races with the app's background sync loop.
-             * @param homeserver the homeserver instance returned by start{Homeserver}
+             *
+             * @param homeserver the homeserver instance returned by {homeserver}Start (e.g. synapseStart).
              */
             stopHomeserver(homeserver: HomeserverInstance): Chainable<AUTWindow>;